# Estimation of the Burden of Iron Deficiency Anemia in France from Iron Intake: Methodological Approach

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## Abstract

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## 1. Introduction

## 2. Methods

#### 2.1. Model Framework for Iron Deficiency Anemia Assessment

- ID appears when iron requirements are not covered by dietary iron.
- The ratio between the proportion of ID and IDA remains constant over the consumption scenarios.
- The consumption of bioavailable dietary iron, such as that found in red meat, reduces IDA.

#### 2.2. Iron Intake Consumption in France

#### 2.3. Prevalence of Iron Deficiency in France

#### 2.4. Prevalence of Iron Deficiency Anemia in France

#### 2.5. Burden of Diseases from Iron Deficiency Anemia

#### 2.6. Second-Order Monte Carlo Simulation

#### 2.7. Consumption Scenarios

## 3. Results

#### 3.1. Prevalence and Number of Iron Deficiencies in France

#### 3.2. Number of Iron Deficiency Anemias

#### 3.3. DALY Attributable to Iron Deficiency Anemias

#### 3.4. Consumption Scenarios

## 4. Discussion

## 5. Conclusions

## Author Contributions

## Funding

## Acknowledgments

## Conflicts of Interest

## Appendix A

#### Appendix A.1. Determination of the Hemoglobin Status in the Population

**Table A1.**Hemoglobin levels values of French population expressed in mean and (standard deviation) extracted from Stoltzfus et al. (2004) and Santé Publique France 2006–2007.

Age Class | Gender (and Status) | Hemoglobin (g/dL) | Reference |
---|---|---|---|

0–4 | Male | 12.5 (1) | [23] |

Female | 12.5 (1) | ||

5–14 | Male | 13.4 (1) | |

Female | 13.4 (1) | ||

15–29 | Male | 14.6 (1) | |

Female | 13.4 (1) | ||

18–24 | Male | 15.5 (0.8) | [26] |

Female (Premenopausal) | 13.5 (1.5) | ||

25–44 | Male | 15.3 (1) | |

Female (Premenopausal) | 13.5 (1.4) | ||

Female (Postmenopausal) | 13.8 (0.6) | ||

45–64 | Male | 15.3 (1.1) | |

Female (Premenopausal) | 13.7 (1.1) | ||

Female (Postmenopausal) | 13.8 (0.9) | ||

65–74 | Male | 14.9 (1.9) | |

Female (Postmenopausal) | 14 (1.2) |

- To determine female hemoglobin level in the age class three to six years old, the linear function was expressed:$$H{b}_{a,g}=0.1173\times meanageoftheclass+12.275$$
- For females, age class from 7 to 11 and from 12 to 17 years old, the average hemoglobin levels were similar and estimated by the fallow function:$$H{b}_{a,g}=-0.0015\times meanageoftheclass+13.413$$
- To determine male hemoglobin level in the age class 3–6, 7–11, and 12–17 years old, the linear function was expressed:$$H{b}_{a,g}=0.1058\times meanageoftheclass+12.331$$

**Table A2.**Hemoglobin levels of the French population expressed in mean and (standard deviation) used in the present study.

Age Class | Gender (and Status) | Hemoglobin (g/dL) |
---|---|---|

3–6 | Male | 12.8 (1) |

Female | 12.7 (1) | |

7–11 | Male | 13.3 (1) |

Female | 13.4 (1) | |

12–17 | Male | 13.9 (1) |

12–14 | Female | 13.4 (1) |

15–17 | Female (Premenopausal) | 13.4 (1) |

18–24 | Male | 15.5 (0.8) |

Female (Premenopausal) | 13.5 (1.5) | |

25–44 | Male | 15.3 (1) |

Female (Premenopausal) | 13.5 (1.4) | |

Female (Postmenopausal) | 13.8 (0.6) | |

45–64 | Male | 15.3 (1.1) |

Female (Premenopausal) | 13.7 (1.1) | |

Female (Postmenopausal) | 13.8 (0.9) | |

65–74 | Male | 14.9 (1.9) |

Female (Postmenopausal) | 14 (1.2) |

#### Appendix A.2. Determining the Proportion of Anemia per Severity

- Proportion of severe anemias:$$An{e}_{a,g,s=severe}=pnorm\left[Hb.{t}_{s=severe},mean\left(H{b}_{a,g}\right),standarddeviation\left(H{b}_{a,g}\right)\right]$$
- Proportion of moderate anemias:$$\begin{array}{l}An{e}_{a,g,s=moderate}=pnorm\left[Hb.{t}_{s=moderate},mean\left(H{b}_{a,g}\right),standarddeviation\left(H{b}_{a,g}\right)\right]-\\ An{e}_{a,g,s=severe}\end{array}$$
- Proportion of mild anemias:$$\begin{array}{ll}An{e}_{a,g,s=mild}=& pnorm\left[Hb.{t}_{s=mild},mean\left(H{b}_{a,g}\right),standarddeviation\left(H{b}_{a,g}\right)\right]\\ & -\left(An{e}_{a,g,s=severe}+An{e}_{a,g,s=moderate}\right)\end{array}$$
- Allocation of anemia severity, among the anemia population$$Alloc.An{e}_{a,g,s}=\frac{An{e}_{a,g,s}}{{\displaystyle \sum}An{e}_{a,g,s}}$$

Red Meat Type | Iron (mg/100 g) |
---|---|

Cooked bourguignon beef | 4.3 |

Cooked stew beef | 4.3 |

Roasted horse meat | 3.4 |

Roasted beef | 3.1 |

Cooked ground beef 5% fat | 2.83 |

Cooked ground beef 10% fat | 2.71 |

Braised beef | 5.9 |

Raw ground beef 5% fat | 2.65 |

Cooked ground beef 15% fat | 2.6 |

Grilled entrecote beef | 2.55 |

Cooked ground beef 20% fat | 2.48 |

Roast beef ribbon | 2.4 |

Burgundy fondue | 2.3 |

Beef grilled steak | 2.21 |

Roasted lamb shoulder | 2.2 |

Cooked dumplings beef | 2.2 |

Beef carpaccio | 1.89 |

Unspecified cooked meat | 1.77 |

Mixed skewer of meat | 1.77 |

Other meat | 1.77 |

Lamb skewer | 1.73 |

Beef skewer | 1.41 |

Roast lamb | 1.4 |

Cooked veal side | 1.3 |

Roasted lean pork tenderloin | 1.29 |

Grilled lamb chop | 1.27 |

Braised ribs | 1.2 |

Breaded veal cutlet | 1.11 |

Roasted loin pork | 1.09 |

Cooked escalope veal | 1 |

Simmered veal | 0.95 |

Roasted tenderloin veal | 0.87 |

Roasted veal | 0.87 |

Grilled pork chop | 0.84 |

Roasted pork | 0.64 |

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**Figure 1.**Flowchart of the assessment model of iron deficiency anemia disease per year in France per age class and gender. White rectangles with dashed line correspond to the “Inputs”, full line to “Intermediate calculation”. Light grey rectangles correspond to the “Final output”. Absorbed iron corresponds to the mean absorbed values provided by European Food Safety Authority (EFSA) considering both heme and non-heme iron.

**Figure 2.**Estimated number of DALY from iron deficiency anemias in France for young children (three to six) and adolescent females (15–17) according to ground beef consumption scenarios. Results expressed per 100,000 individuals per year. Full lines represent the 95% uncertainty around the mean value.

**Figure 3.**Estimated number of DALY from iron deficiency anemias in France for adult males and females according to ground beef consumption scenarios. Results expressed per 100,000 individuals per year. Full lines represent the 95% uncertainty around the mean value.

**Table 1.**Sources of information and implementation of the inputs either as deterministic values or as probability distributions.

Characteristic | Input | Gender ^{1} | Model Implementation Per Age Class ^{2} | Unit | Type ^{3} | From | ||||||||
---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|

3–6 | 7–11 | 12–14 | 15–17 | 18–24 | 25–44 | 45–64 | 65–74 | |||||||

French population data | $Pop$ | Male | 1,571,427 | 1,925,359 | 2,352,805 | 2,788,141 | 8,279,094 | 7,663,979 | 2,269,631 | number | D | [28] | ||

Female Pre-M | 1,498,259 | 1,829,236 | 1,084,687 | 1,159,862 | 2,649,398 | 7,910,584 | 2,694,011 | - | ||||||

Female Post-M | - | - | - | - | - | 157,425 | 5,313,189 | 2,712,349 | ||||||

Iron consumption (absorbed) | Male | $LogN\left(\begin{array}{c}-0.21\\ \left[\begin{array}{c}95\%CI=-0.26\\ -\left(-0.17\right)\end{array}\right],\\ 0.31\\ [95\%CI=0.27\\ -0.36]\end{array}\right)$ | $LogN\left(\begin{array}{c}0.06\\ \left[\begin{array}{c}95\%CI=0.01\\ -0.09\end{array}\right],\\ 0.28\\ [95\%CI=0.26\\ -0.31]\end{array}\right)$ | $LogN\left(\begin{array}{c}0.62\\ \left[\begin{array}{c}95\%CI=0.59\\ -0.66\end{array}\right],\\ 0.34\\ [95\%CI=0.31\\ -0.36]\end{array}\right)$ | $LogN\left(\begin{array}{c}0.52\\ \left[\begin{array}{c}95\%CI=0.46\\ -0.58\end{array}\right],\\ 0.37\\ [95\%CI=0.33\\ -0.42]\end{array}\right)$ | $LogN\left(\begin{array}{c}0.75\\ \left[\begin{array}{c}95\%CI=0.71\\ -0.78\end{array}\right],\\ 0.31\\ [95\%CI=0.29\\ -0.34]\end{array}\right)$ | $LogN\left(\begin{array}{c}0.74\\ \left[\begin{array}{c}95\%CI=0.71\\ -0.78\end{array}\right],\\ 0.32\\ [95\%CI=0.30\\ -0.34]\end{array}\right)$ | $LogN\left(\begin{array}{c}0.79\\ \left[\begin{array}{c}95\%CI=0.75\\ -0.84\end{array}\right],\\ 0.34\\ [95\%CI=0.31\\ -0.37]\end{array}\right)$ | mg/day | U and V | [18] | |||

Female Pre-M | $LogN\left(\begin{array}{c}-0.29\\ \left[\begin{array}{c}95\%CI=-0.34\\ -\left(-0.25\right)\end{array}\right],\\ 0.25\\ [95\%CI=0.21\\ -0.28]\end{array}\right)$ | $LogN\left(\begin{array}{c}-0.07\\ \left[\begin{array}{c}95\%CI=-0.10\\ -\left(-0.03\right)\end{array}\right],\\ 0.29\\ [95\%CI=0.26\\ -0.31]\end{array}\right)$ | $LogN\left(\begin{array}{c}0.43\\ \left[\begin{array}{c}95\%CI=0.38\\ -0.48\end{array}\right],\\ 0.34\\ [95\%CI=0.30\\ -0.37]\end{array}\right)$ | $LogN\left(\begin{array}{c}0.40\\ \left[\begin{array}{c}95\%CI=0.36\\ -0.45\end{array}\right],\\ 0.36\\ [95\%CI=0.33\\ -0.40]\end{array}\right)$ | $LogN\left(\begin{array}{c}0.52\\ \left[\begin{array}{c}95\%CI=0.46\\ -0.58\end{array}\right],\\ 0.37\\ [95\%CI=0.33\\ -0.42]\end{array}\right)$ | $LogN\left(\begin{array}{c}0.59\\ \left[\begin{array}{c}95\%CI=0.56\\ -0.62\end{array}\right],\\ 0.35\\ [95\%CI=0.33\\ -0.37]\end{array}\right)$ | $LogN\left(\begin{array}{c}0.67\\ \left[\begin{array}{c}95\%CI=0.62\\ -0.73\end{array}\right],\\ 0.39\\ [95\%CI=0.35\\ -0.43]\end{array}\right)$ | - | ||||||

Female Post-M | - | - | - | - | - | $LogN\left(\begin{array}{c}0.19\\ \left[\begin{array}{c}95\%CI=-0.09\\ -0.47\end{array}\right],\\ 0.43\\ [95\%CI=0.25\\ -0.63]\end{array}\right)$ | $LogN\left(\begin{array}{c}0.64\\ \left[\begin{array}{c}95\%CI=0.60\\ -0.68\end{array}\right],\\ 0.38\\ [95\%CI=0.35\\ -0.41]\end{array}\right)$ | $LogN\left(\begin{array}{c}0.58\\ \left[\begin{array}{c}95\%CI=0.53\\ -0.64\end{array}\right],\\ 0.34\\ [95\%CI=0.30\\ -0.38]\end{array}\right)$ | ||||||

Iron needs | $IR$ | Male | $N\left(0.5,0.1\right)$ | $N\left(0.8,0.16\right)$ | $N\left(1.27,0.25\right)$ | $N\left(0.97,0.38\right)$ | $N\left(0.97,0.38\right)$ | $N\left(0.97,0.38\right)$ | $N\left(0.97,0.38\right)$ | mg/day | V | [20] | ||

Female Pre-M | $N\left(0.5,0.1\right)$ | $N\left(0.8,0.16\right)$ | $N\left(1.13,0.23\right)$ | $N\left(1.41,0.76\right)$ | $N\left(1.41,0.76\right)$ | $N\left(1.41,0.76\right)$ | $N\left(1.41,0.76\right)$ | |||||||

Female Post-M | - | - | - | - | $N\left(0.97,0.38\right)$ | $N\left(0.97,0.38\right)$ | $N\left(0.97,0.38\right)$ | |||||||

Proportion of iron deficiencies anemia when iron deficiency | $Prop.IDA$ | Male | 0.147 | 0 | 0 | 0 | 0.26 | 0 | 0.42 | number | D | [25,26] | ||

Female Pre-M | 0.147 | 0 | 0 | 0.5 | 0.05 | 0.09 | 0.10 | |||||||

Female Post-M | - | - | - | - | - | 0 | 0 | 0.03 | ||||||

Hemoglobin status | $Hb$ | Male | $N\left(12.8,1\right)$ | $N\left(13.3,1\right)$ | $N\left(13.9,1\right)$ | $N\left(15.5,0.8\right)$ | $N\left(15.3,1\right)$ | $N\left(15.3,1.1\right)$ | $N\left(14.9,1.9\right)$ | g/dL | V | [23,26] | ||

Female Pre-M | $N\left(12.7,1\right)$ | $N\left(13.4,1\right)$ | $N\left(13.4,1\right)$ | $N\left(13.4,1\right)$ | $N\left(13.5,1.5\right)$ | $N\left(13.5,1.4\right)$ | $N\left(13.7,1.1\right)$ | |||||||

Female Post-M | - | - | - | - | - | $N\left(13.8,0.6\right)$ | $N\left(13.8,0.9\right)$ | $N\left(14,1.2\right)$ | ||||||

Hemoglobin threshold for anemia severity | mild | $Hb.t$ | Male | 10.9 | 11.4 | 11.9 | 11.9 | 12.9 | 12.9 | 12.10 | 12.9 | g/dL | D | [4] |

Female | 10.9 | 11.4 | 11.9 | |||||||||||

moderate | Male | 9.9 | 10.9 | 10.9 | 10.10 | 10.9 | ||||||||

Female | 9.9 | 10.9 | ||||||||||||

severe | Male | 7 | 8 | 9 | 8 | |||||||||

Female | 7 | 8 | ||||||||||||

Disability weight | mild | $w$ | Both | $N\left(0.005,0.002\right)$ | number | U | [29] | |||||||

moderate | Both | $N\left(0.058,0.012\right)$ | ||||||||||||

severe | Both | $N\left(0.164,0.030\right)$ |

^{1}Female Pre-M, Premenopausal females; Female Post-M, Postmenopausal females. Menstruating females considered between 15 years and 64 years at most;

^{2}Following R parametrization;

^{3}D, deterministic; V, Variability; U, uncertainty.

**Table 2.**Iron deficiency anemia severity levels and health state descriptions from the Global burden of disease 2013 study [29].

Health State | Health State Description |
---|---|

Mild IDA | Feels slightly tired and weak at times, but this does not interfere with normal daily activities. |

Moderate IDA | Feels moderate fatigue, weakness, and shortness of breath after exercise, making daily activities more difficult. |

Severe IDA | Feels very weak, tired and short of breath, and has problems with activities that require physical effort or deep concentration. |

**Table 3.**Prevalence and number of iron deficiencies per 100,000 French individuals, per age class and gender. Mean value and its 95% confidence interval.

Age Class | Male | Female | ||||
---|---|---|---|---|---|---|

Premenopausal | Postmenopausal | |||||

Prevalence | Number of Cases | Prevalence | Number of Cases | Prevalence | Number of Cases | |

3–6 | 9% (6%–12%) | 220 (140–310) | 9% (7%–13%) | 230 (160–300) | - | - |

7–11 | 20% (16%–24%) | 620 (510–730) | 31% (27%–36%) | 930 (810–1100) | - | - |

12–14 | 15% (13%–18%) | 580 (490–680) | 21% (17%–25%) | 360 (290–440) | - | - |

15–17 | 43.7% (41%–47%) | 820 (760–880) | - | - | ||

18–24 | 9% (6%–12%) | 400 (280–530) | 37% (33%–41%) | 1600 (1400–1700) | - | - |

25–44 | 5% (4%–7%) | 720 (580–880) | 32% (30%–34%) | 4100 (3900–4400) | 34% (17%–50%) | 90 (40–130) |

45–64 | 4% (3%–4%) | 450 (360–460) | 27% (24%–31%) | 1200 (1100–1300) | 8% (7%–10%) | 720 (580–860) |

65–74 | 3.4% (2%–5%) | 130 (80–190) | - | - | 10% (7%–12%) | 420 (320–530) |

**Table 4.**Number of cases and disability adjusted life years (DALY) per 100,000 individuals of iron deficiencies anemias in France, per age class and gender. Mean value and its 95% confidence interval.

Age Class | Male | Female | ||||
---|---|---|---|---|---|---|

Premenopausal | Postmenopausal | |||||

Number of Cases | DALY | Number of Cases | DALY | Number of Cases | DALY | |

3–6 | 32 (21–45) | 0.3 (0.1–0.5) | 33 (23–45) | 0.3 (0.1–0.5) | - | - |

7–11 | 0 (0–0) | 0 (0–0) | 0 (0–0) | 0 (0–0) | - | - |

12–14 | 0 (0–0) | 0 (0–0) | 0 (0–0) | 0 (0–0) | - | - |

15–17 | 404 (377–431) | 4.0 (2.1–5.9) | - | - | ||

18–24 | 0 (0–0) | 0 (0–0) | 77 (69–85) | 1.6 (1.0–2.1) | - | - |

25–44 | 183 (146–224) | 0.9 (0.1–1.8) | 374 (353–394) | 6.5 (4.2–9.0) | 0 (0-0) | 0 (0–0) |

45–64 | 0 (0–0) | 0 (0–0) | 122 (108–136) | 1.2 (0.7–1.8) | 0 (0–0) | 0 (0–0) |

65–74 | 54 (33–80) | 0.6 (0.3–1.0) | - | - | 11 (9–15) | 0.1 (0.1–0.2) |

© 2019 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (http://creativecommons.org/licenses/by/4.0/).

## Share and Cite

**MDPI and ACS Style**

De Oliveira Mota, J.; Tounian, P.; Guillou, S.; Pierre, F.; Membré, J.-M.
Estimation of the Burden of Iron Deficiency Anemia in France from Iron Intake: Methodological Approach. *Nutrients* **2019**, *11*, 2045.
https://doi.org/10.3390/nu11092045

**AMA Style**

De Oliveira Mota J, Tounian P, Guillou S, Pierre F, Membré J-M.
Estimation of the Burden of Iron Deficiency Anemia in France from Iron Intake: Methodological Approach. *Nutrients*. 2019; 11(9):2045.
https://doi.org/10.3390/nu11092045

**Chicago/Turabian Style**

De Oliveira Mota, Juliana, Patrick Tounian, Sandrine Guillou, Fabrice Pierre, and Jeanne-Marie Membré.
2019. "Estimation of the Burden of Iron Deficiency Anemia in France from Iron Intake: Methodological Approach" *Nutrients* 11, no. 9: 2045.
https://doi.org/10.3390/nu11092045