Implications of Vitamin D Status for Children’s Bone Health: A Data Mining Analyses of Observational Studies

ABSTRACT

Objective:

To investigate associations/correlations between bone alterations and vitamin D status in children through data mining analyses based on observational studies.

Material and Methods:

Searches in PubMed, Scopus, Web of Science, and Embase databases were performed to recover studies, published until October 2022, with healthy children, which investigated the vitamin D status, related or not to undesirable bone alterations linked to bone quality (bone mineral density and bone mineral content), fracture or anthropometry. Country, study design, area of expertise (medicine, nutrition, dentistry, others), bone outcome, 25-hydroxyvitamin D data (serum or intake levels), the exams for bone diagnosis, and the results were analyzed in the VantagePoint^TM software.

Results:

Of 20,583 studies, 27 were included. The USA (n=9; 33.3%) had the highest number of publications. Cross-sectional (n=11; 40.7%), case-control (n=9; 33.3%), and cohort studies (n=7; 25.9%) contemplated the medicine and nutritional areas without any study in dentistry. Studies about bone quality (n=21; 77.8%), analyzed through dual-energy X-ray absorptiometry (DXA; n=14; 51.8%), with association (n=16; 59.2%) between the low serum levels of 25-hydroxyvitamin D and undesirable bone alterations (n=14; 51.8%) were the most prevalent.

Conclusion:

Most studies were conducted in the medical area and showed an association between low bone quality and low levels of 25-hydroxyvitamin D, verified through DXA.

Keywords:
Bibliometrics; Vitamin D; Bone Density; Child

Introduction

Vitamin D, also known as "solar vitamin," is a secosteroid [¹] produced in an endogenous form by the skin tissues after solar exposure. It can also be purchased by ingesting specific foods or supplementation [¹,²]. Vitamin D goes through two activation stages, one in the liver and the other in the kidneys. Vitamin D is converted in the liver into hydroxyvitamin D, which is transformed into 1,25-di-hydroxyvitamin D in the kidneys to be metabolically active. Thus, the liver and kidneys are vital in vitamin D activation [³].

One of the main functions of vitamin D is to regulate the amount of calcium and phosphorus in the organism [⁴-⁸], allowing good bone mineralization during early childhood and adolescence, which leads the individual to have stronger bones throughout life [⁹]. In cases of low levels of vitamin D, primarily due to mild hypocalcemia, secondary hyperparathyroidism, osteomalacia, and rickets disease, there is an increase in bone remodeling, with loss of trabecular bone and narrowing of the cortical bone and, therefore, increases the risk of bone deformities and fractures due to minor traumas [⁴].

Considering the harmful effects of low levels of 25-hydroxyvitamin D in children, a significant amount of research has been published concerning its bone effects. Thereby, it is interesting and helpful to researchers in various areas of health, such as medicine, nutrition, and dentistry, to trace a descriptive overview of the observational studies published about the levels of 25-hydroxyvitamin D. This, in turn, enables the design of robust research on what is necessary to advance to obtain scientific evidence on the effect of low 25-hydroxyvitamin D levels on undesirable bone alterations in children.

Therefore, the study aimed to employ data mining and descriptive analyses to provide a quantitative profile of the publications' methods and results on possible associations between vitamin D status in healthy children and undesirable bone alterations involving the medicine, dentistry, and nutritional areas.

Material and Methods

This is a data mining and descriptive analysis of the observational studies published in the literature that were retrieved from a systematic search in electronic databases. Through a quantitative approach, it aimed to provide information to organize and classify some characteristics of the publications, besides identifying patterns and the knowledge of state-of-the-art related to vitamin D status in healthy children associated or not associated with undesirable bone alterations. The study protocol was registered in the Open Science Framework (OSF) database under the DOI 10.17605/OSF.IO/EUA5D.

Search Strategy

Extensive bibliographic research was carried out independently by two researchers (BFA and LJ), assisted by a librarian with experience in systematic searches (DM), who guided the search strategies in the following electronic databases: PubMed, Scopus, Web of Science and Embase in October 2022. We completed the search within the same day to avoid any bias caused by database updates. The search strategy included MeSH terms, synonyms, and accessible terms related to the subject of this review, adapted for each database, without language, date, or publication status restrictions. Thus, keywords were used to search for "observational studies" (S) related to "child" (P), which verified "vitamin D" status (E), associated or not with the "frequency of any diseases" (O). The Boolean operators "AND" and "OR" were applied to combine the terms (Table 1).

Table 1
A search strategy is applied according to each electronic database.

Database	Strategy
PubMed	((Vitamin D[Mesh] OR Vitamin D[Tiab] OR Cholecalciferol[Mesh]) OR Cholecalciferol[Tiab] OR Vitamin D3[Tiab] OR Ergocalciferols[Mesh] OR Ergocalciferol*[Tiab] OR Calcitriol[Mesh] OR Calcitriol[Tiab] OR "dihydroxyvitamin D" AND (child[mesh] OR child*[tiab] OR Child, Preschool[Mesh] OR Infant[mesh] OR Infant*[tiab] OR pre-school*[tiab] OR preschool*[tiab])) AND (observational[tiab] OR Prospective studies[Mesh] OR prospective study[tiab] OR cohort studies[Mesh] OR cohort[tiab] OR follow-up studies[Mesh] OR follow-up study[tiab] OR case-control studies[Mesh] OR case control[tiab] OR retrospective studies[Mesh] OR cross-sectional studies[Mesh] OR cross-sectional[tiab] OR "Disease Frequency"[tiab] OR "prevalence study"[tiab])
Scopus	( ( ( TITLE-ABS-KEY ( "Vitamin D" ) OR TITLE-ABS-KEY ( "dihydroxyvitamin D" ) OR TITLE-ABS-KEY ( cholecalciferol ) OR TITLE-ABS-KEY ( "Vitamin D3" ) OR TITLE-ABS-KEY ( ergocalciferols ) OR TITLE-ABS-KEY ( calcitriol ) ) ) AND ( ( TITLE-ABS-KEY ( child* ) OR TITLE-ABS-KEY ( preschool* ) OR TITLE-ABS-KEY ( pre-school* ) OR TITLE-ABS-KEY ( infant* ) ) ) ) AND ( ( TITLE-ABS-KEY ( observational ) OR TITLE-ABS-KEY ( "prospective study" ) OR TITLE-ABS-KEY ( cohort ) OR TITLE-ABS-KEY ( "follow-up study" ) OR TITLE-ABS-KEY ( "case control" ) OR TITLE-ABS-KEY ( "retrospective study" ) OR TITLE-ABS-KEY ( "cross-sectional" ) OR TITLE-ABS-KEY ( "Disease Frequency" ) OR TITLE-ABS-KEY ( "prevalence study" ) ) )
Web of Science	((TS=(((((("Vitamin D") OR ("dihydroxyvitamin D")) OR (cholecalciferol)) OR ("Vitamin D3")) OR (ergocalciferol)) OR (calcitriol))) AND (TS=((((child*) OR (preschool*)) OR (pre-school*)) OR (infant*)))) AND (TS=(((((((((observational) OR ("prospective study")) OR (cohort)) OR ("follow-up study")) OR ("case-control")) OR ("retrospective study")) OR ("cross-sectional")) OR ("Disease Frequency")) OR ("prevalence study")))
Embase	('vitamin d':ti,ab,kw OR 'dihydroxyvitamin d':ti,ab,kw OR cholecalciferol:ti,ab,kw OR 'vitamin d3':ti,ab,kw OR ergocalciferols:ti,ab,kw OR calcitriol:ti,ab,kw) AND (child*:ti,ab,kw OR 'preschool*':ti,ab,kw OR infant*:ti,ab,kw) AND (observational:ti,ab,kw OR 'prospective study':ti,ab,kw OR cohort:ti,ab,kw OR 'follow up':ti,ab,kw OR 'case control':ti,ab,kw OR 'retrospective study':ti,ab,kw OR 'cross-sectional':ti,ab,kw OR 'disease frequency':ti,ab,kw OR 'prevalence study':ti,ab,kw)

Study Selection

The inclusion criteria were predefined to include only observational studies (cross-sectional, case-control, and cohort studies) about low nutritional and serum 25-hydroxyvitamin D levels in healthy children (0-10 years) [¹⁰] - characterized by the absence of clinical signs/symptoms related to diseases, associated or not to undesirable bone alterations (low bone mineral density, fractures and altered anthropometric measurements). Systematic reviews, case reports, letters to the editor; books and book chapters; clinical trials; studies with adolescents, adults, and the elderly; studies with children with neurological, cognitive, systemic, or chronic diseases; studies that investigated non-osseous outcomes; animal studies, in vitro and in situ studies were excluded. A manual search was also performed in the reference lists of the included studies.

After the searches, all identified studies were imported into a tech-mining and data analysis software (VantagePoint™, version 13.0; Search Technology, Inc.) to remove duplicates. Three independent examiners (BFA, MLM, and LJ) selected the studies by reading the titles and abstracts, applying the eligibility criteria. Studies with insufficient data in the title and abstract were selected for full reading. If the requested information was still not found, the examiners contacted the authors through e-mail. The article was only deleted after five unsuccessful attempts to obtain the missing information. Any disagreement about eligibility was resolved by two experienced researchers (AF and MAV).

Data Extraction and Analyses

The studies were imported into VantagePoint™, and the following variables were assessed in the software itself and also in Microsoft Excel (Microsoft, USA): country (mentioned in the study referring to the first author), authors, journals, area of expertise (medicine, nutrition, dentistry, others), type of study, bone outcome (bone quality - bone mineral density and bone mineral content, fracture and anthropometry), obtaining vitamin D (by ingestion or 25-hydroxyvitamin D serum levels), type of examination performed for bone diagnosis (dual-energy X-ray absorptiometry - DXA, radiography, computed tomography, ultrasound) and results (whether or not there was an association between bone outcome and vitamin D status).

Considering the variable 'country,' all countries of the United Kingdom were counted as a single group, being represented on a world map. A frequency graph also represented countries that included two or more studies. The metrics of the most productive authors (with two or more publications) were represented by a correlation map, which also shows their collaboration (common publications). In addition, a graph was created to represent journals with two or more publications considered the present study's main journals.

Correlation analyses were used for the variables related to the area of expertise and the results of each study. The results were represented by nonlinear graphs (cluster maps), displaying information in 'nodes' linked to each other, creating a cluster. These 'nodes,' represented by small circles, reveal the number of items in a given research group. When two subjects connect to the same node, it means that the studies correlate with the cross-subject. A graph was created to show the results of possible associations between vitamin D status and the type of studies.

Data about the author, the publishing year, the investigated undesirable bone alterations, the performed exams, and the association results of the studies were descriptively presented. In addition, correlation analyses between the undesirable bone alterations and type of examination, results, and means of obtaining vitamin D status were also performed.

Results

The search of the databases initially resulted in 20,583 identified studies, and 9461 duplicates were excluded. After title, abstract, and full-text evaluation, 27 studies were included in this review (Figure 1) [¹¹-³⁷], with general characteristics exemplified in Table 2.

Table 2
Authors and the relationship between vitamin D and the variables investigated in the included studies (n=27).

	Outcome			Vitamin D		Exams					Results
Authors	Bone Quality	Bone Fracture	Anthropometric Measures	Serum levels*	Intake levels	Dual-Energy X-ray Absorptiometry	Radiograph	Peripheral Quantitative Computed Tomography	Ultrasound	No images	Association (Positive or Negative)
Al-Ghamdi et al. [11]	+			+		+			+		º
Breen et al.[12]	+		+	+		+					•
Das et al. [13]			+		+						•
El-Sakka et al. [14]	+		+	+	+	+					º
Filteau et al. [15]	+		+	+					+	•	º
Fu et al. [16]	+			+							º
Garcia et al. [17]	+			+		+					º
Herrmann et al. [18]	+		+	+					+		-
James et al. [19]		+		+						+	+
Mäyränpää et al. [20]	+	+		+		+					+
McVey et al. [21]			+	+		+					-
Mercy et al. [22]			+		+				+		+
Minkowitz et al. [23]		+		+						+	+
Nguyen et al. [24]		+	+	+		+					-
Oladosu et al. [25]		+		+						+	+
Rajakumar et al. [26]	+		+	+	+					+	-
Ren et al. [27]	+	+	+		+	+					+
Ryan et al. [28]	+	+	+	+	+	+					+
Ryan et al. [29]	+	+		+	+	+					-
Ryan et al.[30]	+	+		+		+					-
Ryan et al. [31]	+	+		+		+					+
Sakamoto et al. [32]	+			+			+				+
Sayers et al. [33]	+			+				+			+
Sharawat at al. [34]	+		+	+		+					+
Videhult et al. [35]	+			+	+	+					-
White et al. [36]	+			+		+					-
Yorifuji et al. [37]	+		+	+			+				-

• ^*
  25-hydroxyvitamin D; +With association; -Without association.

Figure 1
Flowchart of the review.

The included studies were conducted in 22 different countries (Figure 2A). The United States of America (n=9; 33.3%) is the country that is most studied on vitamin D and undesirable bone alterations. One multicentric study included different populations (Belgium, Estonia, Germany, Hungary, Italy, Spain, Sweden, and Cyprus). Countries with a more significant number of publications are shown in Figure 2B.

Figure 2
Studies distribution by countries: (a) geographical representation and (b) representation of countries with two or more studies published.

Authors, Publishing Year, and Journals

A total of 185 authors were associated with the 27 included studies published between 2002 and 2022. Considering the first authors of the studies with two or more publications, Ryan L. M. and Tosi, L. were the ones who most published (n=4, for each; 14.8%), followed by Chamberlain J. M., Freishtat R. J., Singer S. A., Teach S. J. and Wood R. (n=3, for each). Ryan L. M., in his four publications, sought associations between fractures in African American children's forearms and low levels of 25-hydroxyvitamin D (serum level ≤20 ng / mL), with the collaboration of 7 authors for publishing these studies. A cooperation network between the authors can be seen in Figure 3, demonstrating the correlation between the authors and the largest number of publications. The Journal of Investigative Medicine (Impact Factor=3.235) owns 3 of the four studies published by Ryan L. M. (Table 3).

Table 3
Frequency of journals with observational studies published about the impact of vitamin D status on children's bone health over the years.

Journal	Years		Total	IF*
	2002-2010	2011-2022
Journal of Investigative Medicine	0	3	3	3.235
Archives of Osteoporosis	0	2	2	3.236
Journal of Pediatric Orthopaedics	0	2	2	2.537
Journal of Clinical Endocrinology and Metabolism	1	1	2	4.756
Archives of Disease in Childhood: Fetal and Neonatal Edition	1	0	1	6.643
BMJ Open	0	1	1	3.007
Bone	0	1	1	4.626
Calcified Tissue International	0	1	1	4.227
Current Pediatric Research	0	1	1	2.05
European Journal of Pediatrics	0	1	1	3.860
Food and Nutrition Bulletin	0	1	1	2.751
Food and Nutrition Research	0	1	1	3.894
International Journal of Pediatrics	0	1	1	-
Journal of Bone and Mineral Research	0	1	1	6.390
Journal of Clinical and Diagnostic Research	0	1	1	1.148
Nutrients	0	1	1	7.185
Oncotarget	0	1	1	2.678
Osteoporosis International	0	1	1	4.507
Pediatrics	0	1	1	7.124
Pediatrics International	0	1	1	1.617
Public Health Nutrition	0	1	1	4.022
The Lancet Diabetes and Endocrinology	0	1	1	44.867

• ^*
  IF: Impact Factor; The International Journal of Pediatrics doesn't have an IF classification.

Figure 3
Authors who published the most studies on the association between low levels of 25-hydroxyvitamin D and undesirable bone alterations in healthy children.

Area of Expertise, Type of Study, and Found Associations/Correlations

Of the 27 observational studies included, 16 (59.2%) were from the medical area, 1 (3.7%) was from the nutritional research, and 10 (37.0%) covered both areas. Of the 16 medicine studies, 11 (40.7%) demonstrated an association, and 5 (18.5%) did not demonstrate an association between vitamin D status and the bone undesirable alterations investigated. The nutritional article did not show an association between the nutritional status of vitamin D and bone alterations. Of the ten studies that contemplated both areas, 5 (50%) demonstrated association, and 5 (50%) had no association, considering the same parameters.

Among the studies, 11 (40.7%) are cross-sectional, 9 (33.3%) are case-control, and 7 (25.9%) are cohort studies. Of the 11 cross-sectional studies, 7 (63.3%) demonstrated an association, and 4 (36.4%) had no association between the investigated bone outcomes and vitamin D status. Of the nine case-controls, 6 (66.7%) demonstrated association, and 3 (33.3%) had no association; and of the seven cohorts research, 3 (42.9%) demonstrated association, and 4 (57.1%) were not associated (Figure 4).

Figure 4
Results of 25-hydroxyvitamin D association by outcomes (a) and study type (b), considering the 27 included studies. The same study could be classified into more than one outcome.

Type of Bone Outcome, 25-hydroxyvitamin D Data, and the Exams’ Type

Among the included studies, 21 (77.8%) analyzed the children's bone quality, of which 12 (57.1%) presented association results between low levels of 25-hydroxyvitamin D and impaired bone quality. Ten studies (37.0%) analyzed bone fracture, of which 7 (70.0%) presented association, demonstrating that low levels of 25-hydroxyvitamin D favors bone fractures. Fourteen (51.8%) studies analyzed anthropometry, of which 7 (50.0%) presented association results between low levels of 25-hydroxyvitamin D and altered anthropometry. It is noteworthy that among the studies, 16 (59.2 %) evaluated more than one bone outcome (Table 2), and two of them evaluated the three investigated outcomes (bone quality, fracture, and anthropometry).

The 25-hydroxyvitamin D data were reported through serum levels in 20 (74.1%) studies and by vitamin D intake through a food consumption frequency questionnaire or dietary recall in only 3 (11.1%). The remaining studies (n=4; 14.8%) investigated serum levels and vitamin D intake using nutritional data.

Of the 14 (51.8%) studies that investigated bone mineral density (BMD) and bone mineral content (BMC) using DXA, total body measurements (excluding the head), lumbar spine (L1-L4), proximal femur, and distal radius were considered. Radiographs were used in two (7.4%) studies to evaluate the association between low levels of 25-hydroxyvitamin D and the child's growth and fracture, performed on the lower limbs (total length), hands, wrist, and ankle. One study chose peripheral quantitative computed tomography (pQCT) to investigate BMD and BMC in the cortical bone of the tibia, measuring bone area and thickness. Quantitative ultrasound (QUS) was used in 4 (14.8%) studies to investigate bone stiffness and BMD of the distal radius, calcaneus, and middle tibia. The studies that did not perform imaging tests (n=6; 22.2%) used questionnaires (n=3; 11.1%) and medical records (n=3; 11.1%) to collect data on the history of patients with fractures (n=4; 14.8%); in addition to anthropometric measurements such as body mass index value (n=2; 7.4%) for growth evaluation.

Discussion

The history of vitamin D began to be investigated in the mid-17th century with the Industrial Revolution. The buildings were made very close to each other, preventing the passage of sunlight and soot from the burning of coal, which polluted the air [²]. Consequently, bone deformities were observed as the main characteristic in children who lived at this time, such as arched legs, pelvic deformation, asymmetric skull, visible appearance of the ends of the ribs next to the sternum bone, spinal deformities, deformations, or delay in the formation of weak and flaccid teeth and legs [⁶]. These effects persisted throughout adulthood, impairing these individuals' quality of life [²]. Precisely because vitamin D is essential for bone metabolism, influencing children's growth, we sought to quantitatively present data from studies investigating possible associations between low 25-hydroxyvitamin D levels and undesirable bone alterations in healthy children. As far as we know, this is the first article that addresses a bibliometric analysis of studies presenting associations between vitamin D status in healthy children with impaired bone quality, fractures, and altered anthropometric measurements.

It was observed that the two main authors who publish on the subject are directly connected through their institutional research groups, with few associations between authors from different institutions. This indicates that the lack of multicenter studies may be a limitation in understanding the results in various populations. The authors of the present study also observed a few studies from developing countries, which may indicate a need for more resources or investment for research in this area. In addition, most studies have been conducted in low-temperature countries, where residents probably do not frequently remain exposed to the sun. In general, 90% to 95% of most people's vitamin D needs are met by frequent exposure to sunlight. Thus, the interest of these countries in studying the association between low 25-hydroxyvitamin D levels and bone complications is justified [²].

About 50 to 100% of European and American children are likely to have vitamin D deficiency, and 97% of African Americans have insufficient serum levels of 25-hydroxyvitamin D [²]. These data may explain the author Ryan L. M.'s interest in the association between fractures of African American children and low levels of 25-hydroxyvitamin D in their studies [²⁸-³¹]. It is also emphasized that dark pigmentation of the skin is considered a risk factor for low levels of 25-hydroxyvitamin D due to a reduced ability to produce this vitamin in the skin [³⁸]. In addition, African American children also have a low diet in vitamin D-rich foods when compared to other ethnic groups [³⁹], which may be associated with socioeconomic factors. Nonetheless, regarding the literature, Asians also presented low levels of 25-hydroxyvitamin D [³⁹]. This can be explained by the sun's zenith angle, as during the winter, people who live further north and south on Earth in relation to the equator are generally unable to produce vitamin D in their skin for up to 6 months of the year [⁴⁰]. Furthermore, these vitamin deficiencies can have multifactorial causes, including diet, genetic, environmental, and economic factors. Therefore, it is necessary to study the status of vitamin D in all individuals in order to seek a balance between diet, sun exposure, and other related factors, regardless of country and season.

The investigated bone outcomes in most studies were bone quality measured through BMD. During early childhood to late adolescence, skeletal mass is continuously accumulated, and around 18 years, 90-95% of bone accumulation seems complete [⁴¹,⁴²]. However, 80% of bone mineral density is genetically determined [⁴²], leaving 20% to be influenced by environmental factors, such as exercise and calcium food intake; low levels of 25-hydroxyvitamin D directly affect skeleton mineralization due to the reduction of the efficiency of intestinal calcium absorption [⁴²]. BMD was the most prevalent measure to evaluate bone quality in studies because it is the most accurate evaluation method [⁴³,⁴⁴].

The authors add that they chose not to specify the type of alterations or diseases in the search strategy so as not to miss any potential study that has investigated some other health condition as the main theme but also reported some bone condition as a secondary outcome.

In this study, it was observed that bone fracture was the outcome of great importance for most authors since 50% of the studies showed an association between low levels of 25-hydroxyvitamin D and bone fracture. Skeletal fractures are responsible for a significant proportion of childhood injuries [⁴⁵,⁴⁶] and result in substantial health costs [⁴⁷,⁴⁸], in addition to the acute consequences of these lesions, including pain and functional limitation [⁴⁹]. Some studies suggest that the high risk of fractures in healthy children stems from lower bone mineralization associated with environmental factors, including low 25-hydroxyvitamin D status (serum level <20 nmol/L) [²⁶], malnutrition such as low calcium intake, low milk intake [⁵⁰] and high body mass index (BMI) [⁵¹,⁵²], physical inactivity, obesity [⁵³,⁵⁴] and genetics [⁵⁵]. Therefore, the lack of food micronutrients, such as vitamin D, could negatively impact the child's bone mineralization process and may lead to future osteoporosis [⁵⁶].

Different tests, such as dual-energy X-ray absorptiometry (DXA), peripheral quantitative computed tomography (pQCT), and quantitative ultrasound (QUS), allow the evaluation of bone mineral density. The results of the present study revealed that the use of DXA was more prevalent (51.8%) concerning other types of imaging exams. This result was probably found because it is an examination that uses two X-ray beams of two different energies to measure bone loss. It is considered the gold standard method for estimating BMD and the risk condition of a bone disease [⁵⁷]. In addition, DXA can represent several regions, such as the entire body, spine, and femur regions. This test is used to diagnose osteoporosis and assess the risk of fracture. It is also used to monitor a given bone therapy [⁵⁷]. However, besides being considered a high-cost test, this method emits a high dose of ionizing radiation to the patient. Especially in children and adolescents, the biological effects caused by ionizing radiation are more present, so the concern with the conscious use of tests that emit radiation is increasingly discussed [⁵⁸], and a criterion when indicating such examination for this age group is recommended.

Peripheral quantitative computed (pQCT) is an imaging technique that uses computerized X-ray attenuation processing to acquire sectional images like a conventional tomography computer. From the cuts is the production of a high-quality model in three dimensions [⁵⁹]. Its use for medical purposes has accelerated in recent years, being used for biological materials studies such as teeth, implants, bones, and, more recently, cartilage. However, it is still practically restricted to scientific research because it is expensive [⁶⁰]. Due to this limitation, we observed that only one study in developed countries used pQCT.

Two-dimensional tests, when compared to tomographic exams, emit a lower radiation dose to the patient [⁶⁰] and, in certain situations, are sufficient to elucidate the diagnosis. Changes in bone microarchitecture or quality caused by low levels of 25-hydroxyvitamin D alter X-ray and thus modify image density and texture [⁶¹]. Therefore, an X-ray becomes a good alternative, being of low cost, easy execution, and fast processing for routine examinations. The authors of the present study also observed that quantitative ultrasound (QUS) was used to determine bone stiffness (14.8%), being a cheaper device with more significant space savings compared to DXA or quantitative computed tomography and does not require the use of ionizing radiation [⁶²]. Moreover, QUS is not only a cheap substitute for measuring BMD, but it can also provide additional information about bone resistance, primarily used to estimate fracture risk [⁶²].

The data about 25-hydroxyvitamin D was investigated through serum levels in most studies, and insufficient or deficient vitamin D intake was investigated through food frequency questionnaires (FFQ) [⁶³] or dietary recalls. The authors of the present study believe that the investigation of vitamin D status through laboratory tests, where serum levels report the results, is more accurate and reliable since, through diet questionnaires, the results depend mainly on the collaboration of the person responsible for the customary investigation of the child's food intake, which can lead to errors or omissions. One reason for these errors is the sex difference that interferes with the reproducibility of FFQs [⁶⁴], suggesting that women have a more stable memory than men [⁶⁵]. This finding is probably explained by the fact that women pay more attention to food intake or because they cook more frequently [⁶⁶]. In addition, children eat meals at school [⁶⁷,⁶⁸], and in some cases, parents are not aware of the intake of certain foods. According to the literature, the report of parents together with children is more accurate than just the individual responses of the parents, emphasizing the value of the child's contribution [⁶⁹]. In this type of evaluation, whose data should be accurate to obtain greater internal validity of the results, using a questionnaire with photos representing the size/quantity of the consumed portion of the food would be interesting. According to some studies, questionnaires with limited categories of answers, provision of memory tips, and evaluation of frequencies or size of the portion through photos make the instrument more accessible and more understandable, resulting in greater data validity [⁷⁰,⁷¹].

Only observational studies, which are subject to reverse causality, were selected for the present review. However, this does not represent a problem since this type of study was chosen for evaluating association/correlation measures rather than the cause-effect relationship. The adopted age range (0-10 years old) was established according to the WHO definition for the group of children [¹⁰]. Several studies were excluded by this criterion, which limited the final number of studies in the present review. However, we limited it to children to reduce variability between studies.

This study presents some limitations, such as no information on exposure to sunlight and sociodemographic data, which could better characterize the sample studied if they were present in the recovered studies. In addition, some studies needed to provide complete information about the collected data, especially those that used medical records information. With this, it was impossible to describe some critical parameters such as the analysis software used, the accuracy of the selected areas in each image, the different regions of the body, and even the type of examination performed to investigate the bone outcome.

In the present review, no study involving healthy children was recovered that investigated a possible association between low 25-hydroxyvitamin D levels and changes in facial bones involving the dentistry area or any other area. This data serves as a warning to dentists since several alterations can affect those bones, affecting the entire stomatognathic system and, consequently, the quality of life of the affected individual due to the increased risk of fracture in the face of a low-impact trauma.

Conclusion

Studies that evaluated a possible association between low 25-hydroxyvitamin D levels and changes in bone quality, fractures, and modified anthropometry in healthy children have been published frequently in recent years, mainly by authors from developed countries. No article on the investigated subject was found in Dentistry. Low 25-hydroxyvitamin D levels were reported by most studies that observed fractures, anthropometric changes, and impaired bone quality in healthy children, who were mainly submitted to dual-energy X-ray absorptiometry for bone evaluation.

Data Availability

The data used to support the findings of this study can be made available upon request to the corresponding author.

• Financial Support
  This study was financed in part by the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior - Brazil (CAPES) - Finance Code 001, by the Fundação de Amparo à Pesquisa do Estado do Rio de Janeiro (FAPERJ), and had financial funding from the Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq) - Finance code 401058/2016-6 - for the VantagePoint™ software.

References

• ^[1]
  Holick MF. Vitamin D deficiency. N Engl J Med 2007; 357(3):266-281. https://doi.org/10.1056/NEJMra070553
  » https://doi.org/10.1056/NEJMra070553
• ^[2]
  Holick MF. Vitamina D. São Paulo: Fundamento Educacional Ltda.; 2012. 352p. [In Portuguese].
• ^[3]
  Fisher L, Fisher A. Vitamin D and parathyroid hormone in outpatients with non-cholestatic chronic liver disease. Clin Gastroenterol Hepatol 2007; 5(4):513-520. https://doi.org/10.1016/j.cgh.2006.10.015
  » https://doi.org/10.1016/j.cgh.2006.10.015
• ^[4]
  Premaor MO, Furlanetto TW. Hipovitaminose D em adultos: Entendendo melhor a apresentação de uma velha doença. Arq Bras Endocrinol Metabol 2006; 50(1):25-37. https://doi.org/10.1590/S0004-27302006000100005 [In Portuguese].
  » https://doi.org/10.1590/S0004-27302006000100005
• ^[5]
  Rosen CJ, Abrams AS, Aloia JF, Brannon PM, Clinton SK, Durazo-Arvizu RA, et al. IOM committee members respond to Endocrine Society vitamin D guideline. J Clin Endocrinol Metab 2012; 97(4):1146-1152. https://doi.org/10.1210/jc.2011-2218
  » https://doi.org/10.1210/jc.2011-2218
• ^[6]
  Shore RM, Chesney RW. Rickets: Part I. Pediatr Radiol 2013; 43(2):140-151. https://doi.org/10.1007/s00247-012-2532-x
  » https://doi.org/10.1007/s00247-012-2532-x
• ^[7]
  Hossein-Nezhad A, Holick MF. Vitamin D for health: A global perspective. Mayo Clin Proc 2013; 88(7):720-755. https://doi.org/10.1016/j.mayocp.2013.05.011
  » https://doi.org/10.1016/j.mayocp.2013.05.011
• ^[8]
  Elder CJ, Bishop NJ. Rickets. Lancet 2014; 383(9929):1665-1676. https://doi.org/10.1016/S0140-6736(13)61650-5
  » https://doi.org/10.1016/S0140-6736(13)61650-5
• ^[9]
  Winzenberg T, Jones G. Vitamin D and bone health in childhood and adolescence. Calcif Tissue Int 2013; 92(2):140-150. https://doi.org/10.1007/s00223-012-9615-4
  » https://doi.org/10.1007/s00223-012-9615-4
• ^[10]
  World Health Organization. Guidelines. Age Groups and Populations. Available from: https://apps.who.int/iris/rest/bitstreams/1336192/retrieve [Accessed on March 17, 2023].
  » https://apps.who.int/iris/rest/bitstreams/1336192/retrieve
• ^[11]
  Al-Ghamdi MA, Lanham-New SA, Kahn JA. Differences in vitamin D status and calcium metabolism in Saudi Arabian boys and girls aged 6 to 18 years: effects of age, gender, extent of veiling and physical activity with concomitant implications for bone health. Public Health Nutr 2012;15(10):1845-53. https://doi.org/10.1017/S1368980011003612
  » https://doi.org/10.1017/S1368980011003612
• ^[12]
  Breen ME, Laing EM, Hall DB, Hausman DB, Taylor RG, Isales CM, et al. 25-hydroxyvitamin D, insulin-like growth factor-I, and bone mineral accrual during growth. J Clin Endocrinol Metab 2011; 96(1):E89-98. https://doi.org/10.1210/jc.2010-0595
  » https://doi.org/10.1210/jc.2010-0595
• ^[13]
  Das S, Sanchez JJ, Alam A, Haque A, Mahfuz M, Ahmed T, et al. Dietary Magnesium, Vitamin D, and Animal Protein Intake and Their Association to the Linear Growth Trajectory of Children from Birth to 24 Months of Age: Results From MAL-ED Birth Cohort Study Conducted in Dhaka, Bangladesh. Food Nutr Bull 2020; 41(2):200-210. https://doi.org/10.1177/0379572119892408
  » https://doi.org/10.1177/0379572119892408
• ^[14]
  El-Sakka A, Penon C, Hegazy A, Elbatrawy S, Gobashy A, Moreira A. Evaluating bone health in Egyptian children with forearm fractures: A case control study. Int J Pediatr 2016; 2016:7297092. https://doi.org/10.1155/2016/7297092
  » https://doi.org/10.1155/2016/7297092
• ^[15]
  Filteau S, Rehman AM, Yousafzai A, Chugh R, Kaur M, Sachdev HP, et al. Associations of vitamin D status, bone health and anthropometry, with gross motor development and performance of school-aged Indian children who were born at term with low birth weight. BMJ Open 2016; 6(1):e009268. https://doi.org/10.1136/bmjopen-2015-009268
  » https://doi.org/10.1136/bmjopen-2015-009268
• ^[16]
  Fu Y, Hu Y, Qin Z, Zhao Y, Yang Z, Li Y, et al. Association of serum 25-hydroxyvitamin D status with bone mineral density in 0-7 year old children. Oncotarget 2016; 7(49):80811-80819. https://doi.org/10.18632/oncotarget.13097
  » https://doi.org/10.18632/oncotarget.13097
• ^[17]
  Garcia AH, Erler NS, Jaddoe VWV, Tiemeier H, van den Hooven EH, Franco OH, et al. 25-hydroxyvitamin D concentrations during fetal life and bone health in children aged 6 years: a population-based prospective cohort study. Lancet Diabetes Endocrinol 2017; 5(5):367-376. https://doi.org/10.1016/S2213-8587(17)30064-5
  » https://doi.org/10.1016/S2213-8587(17)30064-5
• ^[18]
  Herrmann D, Pohlabeln H, Gianfagna F, Konstabel K, Lissner L, Mårild S, et al. Association between bone stiffness and nutritional biomarkers combined with weight-bearing exercise, physical activity, and sedentary time in preadolescent children. A case-control study. Bone. 2015; 78:142-9. https://doi.org/10.1016/j.bone.2015.04.043
  » https://doi.org/10.1016/j.bone.2015.04.043
• ^[19]
  James JR, Massey PA, Hollister AM, Greber EM. Prevalence of hypovitaminosis D among children with upper extremity fractures. J Pediatr Orthop 2013; 33(2):159-62. https://doi.org/10.1097/BPO.0b013e3182770bf7
  » https://doi.org/10.1097/BPO.0b013e3182770bf7
• ^[20]
  Mäyränpää MK, Viljakainen HT, Toiviainen-Salo S, Kallio PE, Mäkitie O. Impaired bone health and asymptomatic vertebral compressions in fracture-prone children: a case-control study. J Bone Miner Res 2012; 27(6):1413-24. https://doi.org/10.1002/jbmr.1579
  » https://doi.org/10.1002/jbmr.1579
• ^[21]
  McVey MK, Geraghty AA, O'Brien EC, McKenna MJ, Kilbane MT, Crowley RK, et al. The impact of diet, body composition, and physical activity on child bone mineral density at five years of age-findings from the ROLO Kids Study. Eur J Pediatr 2020; 179(1):121-131. https://doi.org/10.1007/s00431-019-03465-x
  » https://doi.org/10.1007/s00431-019-03465-x
• ^[22]
  Mercy J, Dillon B, Morris J, Emmerson AJ, Mughal MZ. Relationship of tibial speed of sound and lower limb length to nutrient intake in preterm infants. Arch Dis Child Fetal Neonatal Ed 2007; 92(5):F381-5. https://doi.org/10.1136/adc.2006.105742
  » https://doi.org/10.1136/adc.2006.105742
• ^[23]
  Minkowitz B, Cerame B, Poletick E, Nguyen JT, Formoso ND, Luxenberg SL, et al. Morris-Essex Pediatric Bone Health Group. Low vitamin D lLevels are associated with need for surgical correction of pediatric fractures. J Pediatr Orthop 2017; 37(1):23-29. https://doi.org/10.1097/BPO.0000000000000587
  » https://doi.org/10.1097/BPO.0000000000000587
• ^[24]
  Nguyen PM, Pham LV, Nguyen KT, Nguyen DP, Nguyen HD, Lai NV, et al. Vitamin D and bone mineral density status, and their correlation with bone turnover markers in healthy children aged 6-14 in Vietnam. Curr Pediatr Res 2020; 24(3):204-209.
• ^[25]
  Oladosu MA, Esan O, Oginni LM, Adegbehingbe OO, Adedeji TA. (2021). Predictive value of serum vitamin D3 level for forearm fractures among children in a tropical country: A case control study. J Clin Diag Res 2021; 15(1):RC01-RC04. https://doi.org/10.7860/JCDR/2021/44836.14453
  » https://doi.org/10.7860/JCDR/2021/44836.14453
• ^[26]
  Rajakumar K, Fernstrom JD, Janosky JE, Greenspan SL. Vitamin D insufficiency in preadolescent African American children. Clin Pediatr 2005; 44(8):683-692. https://doi.org/10.1177/000992280504400806
  » https://doi.org/10.1177/000992280504400806
• ^[27]
  Ren J, Brann LS, Bruening KS, Scerpella TA, Dowthwaite JN. Relationships among diet, physical activity, and dual plane dual-energy X-ray absorptiometry bone outcomes in pre-pubertal girls. Arch Osteoporos 2017; 12(1):19. https://doi.org/10.1007/s11657-017-0312-9
  » https://doi.org/10.1007/s11657-017-0312-9
• ^[28]
  Ryan LM, Teach SJ, Brandoli C, Singer SA, Wood R, Freishtat RJ, et al. Predictors of forearm fracture risk in African American children. J Investig Med 2011; 59(3):634-635.
• ^[29]
  Ryan LM, Chamberlain JM, Singer SA, Wood R, Tosi LL, Freishtat RJ, et al. Genetic influences on vitamin D status and forearm fracture risk in African American children. J Investig Med 2012a; 60(6):902-906. https://doi.org/10.2310/JIM.0b013e3182567e2a
  » https://doi.org/10.2310/JIM.0b013e3182567e2a
• ^[30]
  Ryan LM, Teach SJ, Singer SA, Wood R, Freishtat R, Wright JL, et al. Bone mineral density and vitamin D status among African American children with forearm fractures. Pediatrics 2012b; 130(3):e553-560. https://doi.org/10.1542/peds.2012-0134
  » https://doi.org/10.1542/peds.2012-0134
• ^[31]
  Ryan LM, Devaney JM, Gordish-Dressman H, Stevens MW, Tosi L. Clinical factors associated with vitamin d deficiency in African American children with forearm fractures. J Investig Med 2014; 62(4):769-769.
• ^[32]
  Sakamoto Y, Ishijima M, Nakano S, Suzuki M, Liu L, Tokita A, et al. Physiologic leg bowing is not a physiologic condition but instead is associated with vitamin D disorders in toddlers. Calcif Tissue Int 2020; 106(2):95-103. https://doi.org/10.1007/s00223-019-00619-9
  » https://doi.org/10.1007/s00223-019-00619-9
• ^[33]
  Sayers A, Fraser WD, Lawlor DA, Tobias JH. 25-Hydroxyvitamin-D3 levels are positively related to subsequent cortical bone development in childhood: Findings from a large prospective cohort study. Osteoporos Int 2012; 23(8):2117-28. https://doi.org/10.1007/s00198-011-1813-9
  » https://doi.org/10.1007/s00198-011-1813-9
• ^[34]
  Sharawat IK, Dawman L. Bone mineral density and its correlation with vitamin D status in healthy school-going children of Western India. Arch Osteoporos 2019;14(1):13. https://doi.org/10.1007/s11657-019-0568-3
  » https://doi.org/10.1007/s11657-019-0568-3
• ^[35]
  Videhult FK, Öhlund I, Hernell O, West CE. Body mass but not vitamin D status is associated with bone mineral content and density in young school children in northern Sweden. Food Nutr Res 2016; 60:30045. https://doi.org/10.3402/fnr.v60.30045
  » https://doi.org/10.3402/fnr.v60.30045
• ^[36]
  White Z, White S, Dalvie T, Kruger MC, Van Zyl A, Becker P. Bone health, body composition, and vitamin D status of black preadolescent children in South Africa. Nutrients 2019; 11(6):1243. https://doi.org/10.3390/nu11061243
  » https://doi.org/10.3390/nu11061243
• ^[37]
  Yorifuji J, Yorifuji T, Tachibana K, Nagai S, Kawai M, Momoi T, et al. Craniotabes in normal newborns: the earliest sign of subclinical vitamin D deficiency. J Clin Endocrinol Metab 2008; 93(5):1784-8. https://doi.org/10.1210/jc.2007-2254
  » https://doi.org/10.1210/jc.2007-2254
• ^[38]
  Thomas MK, Demay MB. Vitamin D deficiency and disorders of vitamin D metabolism. Endocrinol Metab Clin 2000; 29(3):611-627. https://doi.org/10.1016/s0889-8529(05)70153-5
  » https://doi.org/10.1016/s0889-8529(05)70153-5
• ^[39]
  Moore CE, Murphy MM, Holick MF. Vitamin D intakes by children and adults in the United States differ among ethnic groups. J Nutr 2005; 135(10):2478-2485. https://doi.org/10.1093/jn/135.10.2478
  » https://doi.org/10.1093/jn/135.10.2478
• ^[40]
  Wacker M, Holick MF. Sunlight and Vitamin D: A global perspective for health. Dermatoendocrinol 2013; 5(1):51-108. https://doi.org/10.4161/derm.24494
  » https://doi.org/10.4161/derm.24494
• ^[41]
  Golden NH, Abrams SA. Committee on Nutrition Pediatrics. Optimizing bone health in children and adolescents. Pediatrics 2014; 134(4):e1229-1243. https://doi.org/10.1542/peds.2014-2173
  » https://doi.org/10.1542/peds.2014-2173
• ^[42]
  Stagi S, Cavalli L, Iurato C, Seminara S, Brandi ML, de Martino M. Bone metabolism in children and adolescents: Main characteristics of the determinants of peak bone mass. Clin Cases Miner 2013; 10(3):172-179.
• ^[43]
  Miller PD, Zapalowski C, Kulak CAM, Bilezikian JP. Bone densitometry: The best way to detect osteoporosis and to monitor therapy. J Clin Endocr 1999; 84:1867-1871. https://doi.org/10.1210/jcem.84.6.5710
  » https://doi.org/10.1210/jcem.84.6.5710
• ^[44]
  Baum T, Kutscher M, Muller D, Rath C, Eckstein F, Lochmuller EM, et al. Cortical and trabecular bone structure analysis at the distal radius-prediction of biomechanical strength by DXA and MRI. J Bone Miner Metab 2013; 31(2):212-221. https://doi.org/10.1007/s00774-012-0407-8
  » https://doi.org/10.1007/s00774-012-0407-8
• ^[45]
  Waltzman ML, Shannon M, Bowen AP, Bailey MC. Monkeybar injuries: Complications of play. Pediatrics 1999; 103(5):e58. https://doi.org/10.1542/peds.103.5.e58
  » https://doi.org/10.1542/peds.103.5.e58
• ^[46]
  Stark AD, Bennet GC, Stone DH, Chishti P. Association between childhood fractures and poverty: Population-based study. BMJ 2002; 324(7335):457. https://doi.org/10.1136/bmj.324.7335.457
  » https://doi.org/10.1136/bmj.324.7335.457
• ^[47]
  Galano GJ, Vitale MA, Kessler MK, Hyman JE, Vitale MG. The most frequent traumatic orthopaedic injuries from a national pediatric inpatient population. J Pediatr Orthop 2005; 25(1):39-44. https://doi.org/10.1097/00004694-200501000-00010
  » https://doi.org/10.1097/00004694-200501000-00010
• ^[48]
  Rodriguez-Merchan EC. Pediatric skeletal trauma: A review and historical perspective. Clin Orthop Relat Res 2005; 432:8-13.
• ^[49]
  Beaty JH, Rockwood CA, Kasser JR. Rockwood and Wilkins Fractures in Children. 7th ed. Philadelphia, PA: Wolters Kluwer/Lippincott, Williams & Wilkins; 2010, 292-444.
• ^[50]
  Goulding A, Grant AM, Williams SM. Bone and body composition of children and adolescents with repeated forearm fractures J Bone Miner Res 2005; 20(12):2090-2096. https://doi.org/10.1359/JBMR.050820
  » https://doi.org/10.1359/JBMR.050820
• ^[51]
  Goulding A, Cannan R, Williams SM, Gold EJ, Taylor RW, Lewis-Barned NJ. Bone mineral density in girls with forearm fractures. J Bone Miner Res 1998; 13(1):143-148. https://doi.org/10.1359/jbmr.1998.13.1.143
  » https://doi.org/10.1359/jbmr.1998.13.1.143
• ^[52]
  Goulding A, Jones IE, Taylor RW, Williams SM, Manning PJ. Bone mineral density and body composition in boys with distal forearm fractures: A dual-energy x-ray absorptiometry study. J Pediatr 2001; 139(4):509-515. https://doi.org/10.1067/mpd.2001.116297
  » https://doi.org/10.1067/mpd.2001.116297
• ^[53]
  Lehtonen-Veromaa MK, Möttönen TT, Nuotio IO, Irjala KM, Leino AE, Viikari JS. Vitamin D and attainment of peak bone mass among peripubertal Finnish girls: A 3-y prospective study. Am J Clin Nutr 2002; 76(6):1446-1453. https://doi.org/10.1093/ajcn/76.6.1446
  » https://doi.org/10.1093/ajcn/76.6.1446
• ^[54]
  Ma D, Jones G. The association between bone mineral density, metacarpal morphometry, and upper limb fractures in children: A population-based case-control study. J Clin Endocrinol 2003; 88(4):1486-1491. https://doi.org/10.1210/jc.2002-021682
  » https://doi.org/10.1210/jc.2002-021682
• ^[55]
  Fischer PR, Thacher TD, Pettifor JM, Jorde LB, Eccleshall TR, Feldman D. Vitamin D receptor polymorphisms and nutritional rickets in Nigerian children. J Bone Miner Res 2000; 15(11):2206-2210. https://doi.org/10.1359/jbmr.2000.15.11.2206
  » https://doi.org/10.1359/jbmr.2000.15.11.2206
• ^[56]
  NIH. Consensus development panel on osteoporosis prevention, diagnosis, and therapy. Osteoporosis prevention, diagnosis, and therapy. J Am Med Assoc 2001; 285(6):785-795. https://doi.org/10.1001/jama.285.6.785
  » https://doi.org/10.1001/jama.285.6.785
• ^[57]
  Choi YJ. Dual-energy x-ray absorptiometry: Beyond bone mineral density determination. Endocrinol Metab 2016; 31(1):25-30. https://doi.org/10.3803/EnM.2016.31.1.25
  » https://doi.org/10.3803/EnM.2016.31.1.25
• ^[58]
  ICRP. The 2007 Recommendations of the International Commission on Radiological Protection. ICRP publication 103. Annals of the ICRP 2007; 37(2-4):1-332. https://doi.org/10.1016/j.icrp.2007.10.003
  » https://doi.org/10.1016/j.icrp.2007.10.003
• ^[59]
  Bouxsein ML, Boyd SK, Christiansen BA, Guldberg RE, Jepsen KJ, Muller R. Guidelines for assessment of bone microstructure in rodents using micro-computed tomography. J Bone Miner Res 2010; 25(7):1468-1486. https://doi.org/10.1002/jbmr.141
  » https://doi.org/10.1002/jbmr.141
• ^[60]
  Cheung AM, Adachi JD, Hanley DA, Kendler DL, Davison KS, Josse R, et al. High-resolution-peripheral quantitative computed tomography for the assessment of bone strength and structure: a review by the Canadian Bone Strength Working Group. Curr Osteoporos Rep 2013; 11(2):136-146. https://doi.org/10.1007/s11914-013-0140-9
  » https://doi.org/10.1007/s11914-013-0140-9
• ^[61]
  Eckstein F, Matsuura M, Kuhn V, Priemel M, Müller R, Link TM, et al. Sex differences of human trabecular bone microstructure in aging are site-dependent. J Bone Miner Res 2007; 22(6):817-824. https://doi.org/10.1359/jbmr.070301
  » https://doi.org/10.1359/jbmr.070301
• ^[62]
  Barkmann R, Glüer CC. Quantitativer Ultraschall. Der Radiologe 2006; 46(10):861-869. https://doi.org/10.1007/s00117-006-1394-3
  » https://doi.org/10.1007/s00117-006-1394-3
• ^[63]
  Sichieri R, Everhart J. Validity of a Brazilian food frequency questionnaire against dietary recalls and estimated energy intake. Nutr Res 1998; 18(10):1649-1659. https://doi.org/10.1016/S0271-5317(98)00151-1
  » https://doi.org/10.1016/S0271-5317(98)00151-1
• ^[64]
  Cui Q, Xia Y, Wu Q, Chang Q, Niu K, Zhao Y. A meta-analysis of the reproducibility of food frequency questionnaires in nutritional epidemiological studies. Int J Behav Nutr Phys Act 2021; 18(1):12. https://doi.org/10.1186/s12966-020-01078-4
  » https://doi.org/10.1186/s12966-020-01078-4
• ^[65]
  Tsubono Y, Kobayashi M, Sasaki S, Tsugane S, JPHC. Validity and reproducibility of a self-administered food frequency questionnaire used in the baseline survey of the JPHC study cohort I. J Epidemiol 2003; 13(1 Suppl):S125-S133. https://doi.org/10.2188/jea.13.1sup_125
  » https://doi.org/10.2188/jea.13.1sup_125
• ^[66]
  Männistö S, Virtanen M, Mikkonen T, Pietinen P. Reproducibility and validity of a food frequency questionnaire in a case-control study on breast cancer. J Clin Epidemiol 1996; 49(4):401-409. https://doi.org/10.1016/0895-4356(95)00551-X
  » https://doi.org/10.1016/0895-4356(95)00551-X
• ^[67]
  Johnson L, Mander A, Jones L, Emmett P, Jebb S. A prospective analysis of dietary energy density at age 5 and 7 years and fatness at 9 years among UK children. Int J Obes 2008; 12(4):586-593. https://doi.org/10.1038/sj.ijo.0803746
  » https://doi.org/10.1038/sj.ijo.0803746
• ^[68]
  Auld CRG, Heimendinger J, Hambidge C, Hambidge M. Outcomes from a school-based nutrition education program using resource teachers and cross-disciplinary models. J Nutr Educ 1998; 12(10):268-280. https://doi.org/10.1016/S0022-3182(98)70336-X
  » https://doi.org/10.1016/S0022-3182(98)70336-X
• ^[69]
  Eck L, Klesges R, Hanson C. Recall of a child’s intake from one meal: Are parents accurate? J Am Diet Assoc 1989; 12(6):784-789.
• ^[70]
  Cade J, Thompson R, Burley V, Warm D. Development, validation and utilisation of food-frequency questionnaires - A review. Public Health Nutr 2002; 5(4):567-587. https://doi.org/10.1079/phn2001318
  » https://doi.org/10.1079/phn2001318
• ^[71]
  Rezazadeh A, Omidvar N, Tucker KL. Food frequency questionnaires developed and validated in Iran: A systematic review. Epidemiol Health 2020; 42:e2020015. https://doi.org/10.4178/epih.e202001
  » https://doi.org/10.4178/epih.e202001

Edited by

Academic Editor: Alessandro Leite Cavalcanti

Publication Dates

• Publication in this collection
  24 May 2024
• Date of issue
  2024

History

• Received
  22 Mar 2023
• Reviewed
  05 July 2023
• Accepted
  01 Oct 2023