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Endocrine, Metabolic & Immune Disorders - Drug Targets, 2022, 22, 38-48
RESEARCH ARTICLE
ISSN: 1871-5303
eISSN: 2212-3873

Dietary Intakes and Food Habits of Wheelchair Basketball Athletes Com- Impact
Factor:
2.895

pared to Gym Attendees and Individuals who do not Practice Sport Activ-
ity The official journal of the ITALIAN ASSOCIATION OF CLINICAL
ENDOCRINOLOGISTS, shortly defined AME
(Associazione Medici Endocrinologi)

Elisabetta Toti1, Valentina Cavedon2, Anna Raguzzini1, Anna Lucia Fedullo1, Chiara Milanese2,
Elisabetta Bernardi3, Sheila Bellito4, Marco Bernardi4,5, Tommaso Sciarra6 and Ilaria Peluso1,*
Endocrine, Metabolic & Immune Disorders -Drug Targets

1
Research Centre for Food and Nutrition, Council for Agricultural Research and Economics (CREA-AN), Rome, Italy;
2
Department of Neurosciences, Biomedicine and Movement Sciences, University of Verona, Verona, Italy; 3Depart-
ment of Biosciences, Biotechnologies and Biopharmaceutics, University of Bari “Aldo Moro,” Bari, Italy; 4Feder-
azione Italiana Pallacanestro In Carrozzina (FIPIC), Rome, Italy; 5Department of Physiology and Pharmacology “V.
Erspamer”, Sapienza University of Rome, Italy; 6Joint Veteran Center, Scientific Department, Army Medical Center,
Rome, Italy

Abstract: Background: Mediterranean diet (Med-D) has been previously suggested for athletes,
but Paralympics usually have a low intake of plant foods. Orthorexia nervosa (ON) can drive die-
tary intake of both athletes and gym attendees.

Objective: We aimed to compare dietary intakes and food habits of elite wheelchair basketball ath-
letes (WBA) and able-bodied individuals who practice or not sport activity and with different fat
mass percentage (FM%).

Methods: We recruited 15 WBA from the Italian National team and 3 control groups (15 each
group): healthy individuals who do not practice any sports activity (NSA) and gym attendees with
ARTICLE HISTORY
low (GAL, FM%<17) and high (GAH, FM%>18) FM%. Food consumption was monitored by a 3-
Received: August 25, 2020 d diary, while Med-D scores and ON score were evaluated through standardized questionnaires. In
Revised: November 30, 2020 WBA we also assessed Neurogenic Bowel Dysfunction (NBD), GastroEsophageal Reflux Disease
Accepted: December 11, 2020
(GERD), allergy questionnaire for athletes (AQUA) and Starvation Symptoms Inventory (SSI).
DOI:
10.2174/1871530321666210208213046 Results: In WBA, ON correlated with GERD and SSI. WBA and GAH with eating behavior of ON
had higher adherence to Med-D, whereas NSA had less adherence to Med-D. Sub-score, including
fruits, vegetables and legumes, was higher in the GAL and GAH groups compared to the WBA and
NSA groups. Med-D was inversely related to animal protein intake (PRO-AN) in NSA and GAL.
FM% was inversely related to PRO-AN in WBA and GAH, and to ON only in GAH. In WBA,
PRO-AN and vegetable protein intake correlated with both carbohydrate and energy intakes.

Conclusion: In WBA, commitment to wellness (ON and Med-D adherence) could be a response to
gastrointestinal and starvation symptoms. WBA should be involved in setting their own individual-
ized dietary strategies.

Keywords: Body composition, dietary habit, Mediterranean diet, nutrition, paralympics, starvation symptoms, sport, spinal
cord injury, spina bifida, wheelchair sport.

1. INTRODUCTION behavioral dimensions of the drive for muscularity [2]. Al-


though ON emerged as a predictor of muscle dysmorphia
Strict control of food intake is a feature of orthorexia ner-
symptoms in bodybuilders [4], controversy in the field of
vosa (ON), which is common in gym attendees [1], and it is
ON exists, especially when physical health status drives eat-
associated with frequent exercising [1], exercise dependence
ing behavior (including food restriction to relieve constipa-
[2], dissatisfaction with their own body appearance [3] and
tion) [5].
Paralympic sports are practised by athletes with various
* Address correspondence to this author at the Research Centre for Food health conditions [6], including those with spinal cord injury
and Nutrition, Council for Agricultural Research and Economics (CREA-
AN), Via Ardeatina 546, Rome, Italy; Tel/Fax: +39- 06 51494 426; (SCI) and spina bifida (SB). Neurogenic bowel dysfunction
E-mail: ilaria.peluso@crea.gov.it (NBD), which has a high prevalence in individuals with SCI

2212-3873/22 $65.00+.00 © 2022 Bentham Science Publishers


Dietary Intakes and Food Habits Endocrine, Metabolic & Immune Disorders - Drug Targets, 2022, Vol. 22, No. 1 39

and SB, induces symptoms that affect dietary intake Starvation symptoms in the “starvation symptom invento-
(amount or type of food consumed) [7]. ry” (SSI) questionnaire include preoccupation with food and
Although the Mediterranean diet (Med-D) has been eating, impaired cognitive performance, poor emotional and
suggested as a natural supplemental resource [8] for able- social functioning and physiological changes [18].
bodied athletes [9] and for veterans with injuries [10], Para- For all volunteers, the degree of adherence to the Med-D
lympic athletes have a low-quality diet, in terms of fruits, diet was calculated with: the 14-item Mediterranean Diet
vegetables, legumes and cereals [11]. However, a low-fibre Score (MDS), the 11 items MEDScore and sub-scores (co-
diet could be beneficial in managing NBD in SCI [12]. herent - CO, incoherent - IC and different - D), as previously
The study hypothesis was that the dietary habits of Para- described [19].
lympic athletes could be due to health conditions rather than ORTO-15 was used for ON evaluation [20] and sub-
to ON. scores ORTO-12 (excluded items: 5, 6, 8) [21], ORTO-11
In this comparative study, we aimed to compare the ad- (excluded items: 5, 8, 14, 15) [22], ORTO-9 (excluded
items: 1, 2, 8, 9, 13, 14) [23], ORTO-7 (excluded items: 2,
herence to Med-D, the occurrence of ON and the dietary in-
5, 6, 8, 10, 12, 14, 15) [24] and ORTO-6 (excluded items:
takes in elite wheelchair basketball athletes (WBA) with re-
1,2, 5, 6, 8, 9, 13, 14 and 15) [25] were calculated.
spect to healthy individuals who do not practice sports activi-
ty and gym attendees with different fat mass percentage Habitual dietary intake was assessed by means of a vali-
(FM%). dated 3-day recall record questionnaire, two consecutive
working days, and one-weekend day/holiday as described by
2. MATERIALS AND METHODS Willett [26] and additional information was acquired during
a nutritional interview performed by an experienced dieti-
2.1. Recruitment of Volunteers and Inclusion Criteria tian. The nutritional composition of the diet was calculated
The sample included 15 male WBA of the Italian using the CREA-AN tables of the composition of foods [http-
National team, during a training camp before the 2019 Euro- s://www.crea.gov.it/-/tabella-di-composizione-degli-
alimenti] and the USDA Databases [https://ndb.nal.usda.gov-
pean Championship. The International Wheelchair Basket-
/ndb/].
ball Federation (IWBF) classification documents, ASIA
(American Spinal Injury Association Impairment Scale) and 2.3. Statistical Analysis
health condition of each WBA were provided by the “Feder-
azione Italiana Pallacanestro in Carrozzina” (Rome, Italy). Significance among groups for categorical variables
were assessed by χ2 probability test. Continuous variables
We selected control healthy able-bodied individuals were expressed as means and standard error of the mean
(Body Mass Index: BMI range from 20 to 30 kg/m2), from a (SEM).
no-profit study (Research Centre for Food and Nutrition,
Council for Agricultural Research and Economics, Rome, Analysis of variance (ANOVA) (Normality Test Passed)
Italy), according to the following exclusion criteria: any dis- or ANOVA on Ranks (Normality Test Failed), followed by
ease, allergy, food intolerance, special diets or dietary restric- Student-Newman-Keuls post hoc analysis, were used for
tion (including vegetarian diet). comparing the groups. Spearman correlations were assessed
between the parameters of interest.
Based on the FM%, determined by skinfold thickness
[13], three groups of controls (15 male each) were selected, The level of significance was set at P <0.05. All statisti-
including inactive men not practicing any sports activity cal tests were performed using Sigma plot software (Jandel
(NSA) and gym attendees with FM% lower than 17% Scientific, Inc.).
(GAL) and higher than 18% (GAH).
3. RESULTS
2.2. Characteristics of Volunteers
3.1. Characteristics of Volunteers
Data characterizing the volunteers was collected through
Health condition of WBA is reported in Table 1.
questionnaires. Potential confounders, including smoking
habits, diseases and use of drugs, were determined. For According to the drugs used (Table 1): one WBA took in-
WBA, according to Krogh et al. [14], we calculated the per- sulin (because of diabetes), one WBA took oxycodone (be-
centages of athletes with severe (score ≥14), moderate cause affected by chronic pain) and three took oxybutynin
(score ranging between 10–13) and minor (score ranging be- (because of the neurogenic bladder).
tween 7–9) NBD scores. The “gastroesophageal reflux dis- The IWBF class ranged between 1-4.5 and Spearman cor-
ease” (GERD) score was calculated according to Ubaldi et relation analysis revealed a significantly high correlation be-
al. [15]. tween IWBF class and NBD (-0.754, p<0.001). Being IWBF
The “allergy questionnaire for athletes” (AQUA) was class a reverse score, WBA with higher impairment had
used to evaluate the percentage of WBA with allergy more NBD symptoms. However, the major symptoms were
(score≥5) [16] and the reported upper respiratory tract infec- related to constipation and were not reported only in WBA
tions and herpes labialis [17]. with SCI. Mean SSI of WBA (Table 1) was within the range
40 Endocrine, Metabolic & Immune Disorders - Drug Targets, 2022, Vol. 22, No. 1 Toti et al.

Table 1. Characteristics of WBA.

Amputation n=5: TF (L), TF (R), TF (L and R), TT (R), TF (L and R) plus TR (R).
SB n=1: ASIA A – Lum 2 (R and L).
SCI n=6: ASIA A - Lum 2 (R) T11 (L),
ASIA A - T1 (R) T2 (L),
Health condition/ ASIA A - T10 (R and L),
Impairment ASIA A - T12 (R and L),
ASIA A - T4 (R and L),
ASIA D – Lum 1 (R and L).
OHC n=3: different length plus extra-rotation (L), foot amelia/dismelia (R and L) and impaired strength and range of motion in the lower
limb (R).
Drugs
Insulin 1/15
Oxycodone 1/15
Oxybutynin 3/15
NBD score: 5.5±1.5
Severe ≥14 1/15
Moderate 4/15
Minor 7–9 2/15
GERD score: 3.9±0.1
SSI score: 8.5±1.6
> 20.1 1/15
AQUA score: 5.5±1.6
>5 7/15
WBA: wheelchair basketball athletes; SCI: spinal cord injury; SB: spina bifida; OHC: other health conditions; ASIA: American Spinal Injury Association Impairment Scale. Lum:
lumbar; T: thoracic; L: left; R: right; LLA: lower limb amputation; ULA: upper limb amputation; TF: transfemoral; TT: transtibial; TR: trans-radial; NBD: neurogenic bowel dysfunc-
tion; GERD: gastroesophageal reflux disease; SSI: starvation symptoms inventory; AQUA: allergy questionnaire for athletes.

Table 2. Comparison of WBA and control groups.

WBA NSA GAL GAH


Age (years) 28.5±1.5 31.5±2.2 30.1±2.2 31.8±2.0
BM (kg) 74.8±3.2 79.5±2.5 82.5±2.2 81.7±2.2
FM% 21.8±1.2 (a) 24.9±2.0 (a) 13.5±0.7 (b) 23.5±1.5 (a)
Training (h/week) 14.8±1.6 (a) 0 3.9±0.5 (b) 2.5±0.5 (b)
Sitting* (h/week) 78.6±3.9 (a) 40.1±3.9 (b) 33.1±3.2 (b) 36.4±3.3 (b)
Smokers 2/15 3/15 3/15 4/15
Occasionally 2/15 3/15 2/15 6/15
Alcohol drinkers 13/15 9/15 10/15 10/15
WBA: wheelchair basketball athletes; GAL: gym attendees with FM% below 17; GAH: gym attendees with FM% above 18; NSA: inactive men who do not practice sport activity.
NA: not applicable; BM: body mass; FM%: fat mass percentage; *for WBA meal and screen (television/PC) time. Continuous variables are expressed as means with SEM, Student-
Newman-Keuls.: (a) versus (b) p<0.05. Categorical variables χ2: (a) versus (b) p<0.05.

reported in healthy individuals (10.4 ± 9.7) and only one had On the other hand, WBA spent more time in training and
a score above the cutoff [18]. in a sedentary state (Table 2). In both GAL and GAH
groups, 4 out of 15 gym attendees practised bodybuilding
Other conditions were revealed by GERD impact scale and the others practised both strength and aerobic training.
(reverse score, correlated with SSI -0.643, p<0.01) and
AQUA score (Table 1). WBA, GAL and GAH used protein supplements, with a
mean intake of 19.3±2.4, 27.3±6.5 and 29.3±12.2 g/d, re-
In the AQUA questionnaire, 5/15 WBA declared to have spectively. No differences were found for age and smoking
Herpes labialis 1 to 3 times/year and 6/15 to give up training (Table 2). All volunteers were occasional drinkers and dur-
or competitions for an infectious episode (1-3/year). ing the 3d-food diary 9 WBA, 8 NSA, 3 GAL and 10 GAH
On the contrary, according to the exclusion criteria indi- reported drinking alcoholic beverages with a mean alcohol
viduals of the control groups were free of any disease and intake of: 4.1±1.2, 8.2±2.7, 15.8±4.4, 7.3±1.5 g/d, respective-
did not take any drug. ly.
BMI did not differ significantly among the control Habitual dietary intakes are reported in Table 3. Percent-
groups (kg/m2: 25.8±0.7, 25.7±0.5 and 25.6±0.6 for NSA, age of energy intake (En) from alcoholic beverages was high-
GAL and GAH, respectively), whereas according to the in- er in GAH compared to WBA.
clusion criteria, FM% was lower in GAL compared to the En% from macronutrients (Table 3) did not comply with
other control groups and to WBA (Table 2). the energy intake for habitual diet for sport characterized by
Dietary Intakes and Food Habits Endocrine, Metabolic & Immune Disorders - Drug Targets, 2022, Vol. 22, No. 1 41

Table 3. Energy, macronutrients and fiber intakes.

WBA NSA GAL GAH


En Kcal/kg BM/d 32.6±2.8 28.4±2.8 30.2±1.2 28.5±1.1
Fat % En 36.9±0.6 33.7±1.5 32.4±1.6 35.7±1.0
>35% 10/15 11/15 7/15 8/15
>25% 15/15 13/15 12/15 15/15
CHO % En 43.9±1.2 (a) 50.1±1.3 (b) 41.4±2.6 (a) 43.1±2.5 (a)
<45 * 8/15 1/15 9/15 6/15
<55 15/15 13/15 14/15 15/15
<57 15/15 13/15 14/15 15/15
Sugars %En 14.9±1.1 (a) 11.1±1.3 (a,b) 8.8±1.2 (b) 8.4±0.9 (b)
>15% En 7/15 2/15 1/15 0/15
CHO g/kg BM 3.6±0.3 3.6±0.2 3.1±0.3 3.0±0.2
<2g/kg BM 1/15 0/15 2/15 1/15
Proteins %En: 18.4±0.7 (a) 14.8±0.8 (b) 25.3±1.9 (c) 19.7±2.4 (a)
>20% ** 4/15 1/15 11/15 5/15
>18% ** 9/15 2/15 12/15 5/15
PROT-AN 65.8±1.9 62.1±1.4 65.3±2.4 62.9±2.3
PROT-VEG 30.4±1.8 (a) 37.8±1.4 (b) 23.3±2.5 (c) 32.2±3.2 (a)
PROT-SUP 3.7±1.7 (a) 0 11.0±2.9 (b) 4.8±2.5 (a)
Proteins g/kg BM 1.5±0.1 (a) 1.0±0.1 (b) 1.9±0.1 (c) 1.4±0.1 (a)
<0.9 g/kg 2/15 3/15 0/15 4/15
<1.2 g/k*** 6/15 13/15 0/15 8/15
>1.7 g/kg** 4/15 0/15 9/15 5/15
>2.0 g/kg* 3/15 0/15 7/15 4/15
PROT-AN 0.9±0.08 (a) 0.6±0.02 (b) 1.2±0.1 (c) 0.9±0.1 (a)
PROT-VEG 0.4±0.1 0.4±0.1 0.4±0.1 0.4±0.1
Alcohol %En 0.7±0.2 (a) 0.8±0.3 (a,b) 0.8±0.5 (a,b) 1.4±0.4 (b)
Fibre (gr/d) 17.4±1.3 (a) 19.1±1.3 (a) 20.2±2.1 (a,b) 23.4±1.1 (b)
<25g/d 14/15 13/15 12/15 13/15
WBA: wheelchair basketball athletes; GAL: gym attendees with FM% below 17; GAH: gym attendees with FM% above 18; NSA: inactive men who do not practice sport activity.
En: energy intake; CHO: carbohydrates; PROT-AN: proteins from animal sources; PROT-VEG: proteins from vegetable sources; PROT-SUP: proteins from supplements. Continu-
ous variables are expressed as means with SEM. Student-Newman-Keuls: multiple comparison (a), (b) and (c): p<0.05. Categorical variables, χ2: *p<0.05, **p<0.01, ***p<0.001.

a mixed (aerobic and anaerobic) metabolism, including bas- Although WBA had a higher percentage of sugars’ in-
ket (carbohydrates: CHO 57%, fat 25% and protein 18%) take, in 7/15 above the suggested dietary target (<15%En),
and for power sport (CHO 55%, fat 25% and protein 20%), one of them had a CHO intake below the LARN suggested
suggested by the Federazione Medico Sportiva Italiana target in order to prevent ketosis (2g/kg BM/d).
(https://www.nutrizioneesalute.fmsi. it/images/img/pdf/opus- GAL was the group with the highest intake of proteins
colo_per_atleti_e_famiglie.pdf). (g/kg BM/d), especially from animal and supplement
sources while in the WBA and in both the gym attendees’
Furthermore, in some cases macronutrients’ intake did
groups, different percentages of volunteers had low or high
not comply with the recommended intakes for the Italian intakes compared to the recommendations (Table 3).
population [Livelli di Assunzione di Riferimento di Nutrien-
ti ed energia per la popolazione italiana (LARN), https://sin- Despite mean intakes of micronutrients were in the
u.it/tabelle-larn-2014/] (CHO at least 45%, sugars below range of the LARN, many volunteers, in all groups, had in-
15%, fat below 35%, proteins 0.9g/kgBM/d). takes below the recommended values for calcium and vita-
mins D, A and B12 (Table 4). In particular, all WBA had vi-
Means of fat% were higher compared to the suggested tamin D intakes below the recommended values and the
values in all groups, whereas CHO % was higher in the mean intake was lower in WBA compared to the other
NSA compared to WBA, GAL and GAH (Table 3). groups (Table 4). Furthermore, more WBA (9/15) than GAL
42 Endocrine, Metabolic & Immune Disorders - Drug Targets, 2022, Vol. 22, No. 1 Toti et al.

Table 4. Micronutrients intakes.

WBA NSA GAL GAH


Vitamin B1 mg 1.3±0.2 1.4±0.2 1.6±0.1 1.6±0.1
<1.2 9/15 6/15 3/15 4/15
Vitamin B2 mg 1.9±0.3 1.8±0.1 2.2±0.2 2.0±0.1
<1.6 * 9/15 6/15 2/15 3/15
Vitamin B6 mg 2.4±0.2 (a) 1.4±0.1 (b) 1.7±0.1 (b) 1.4±0.1 (b)
<1.3 0/15 5/15 4/15 5/15
Vitamin B12 µg 2.2±0.1 1.9±0.1 2.1±0.1 1.9±0.1
<2.4 12/15 13/15 12/15 13/15
Vitamin C mg 99±13 104±14 130±11 108±10
<105 10/15 7/15 5/15 6/15
Vitamin E mg 14.8±0.8 13.2±1.0 16.9±1.1 15.7±1.1
<13 4/15 7/15 3/15 3/15
Vitamin A (RE) µg 928±184 (a) 504±29 (b) 627±39 (b) 578±44 (b)
<700 * 9/15 15/15 10/15 12/15
Vitamin D µg 3.6±0.9 (a) 12.5±1.1 (b) 13.6±0.6 (b) 14.2±0.7 (b)
<15 15/15 11/15 11/15 11/15
Calcium mg 759±107 856±22 859±38 935±62
<1000 12/15 14/15 11/15 11/15
Iron mg 12.2±0.9 12.7±1.1 12.8±0.8 12.2±0.6
< 10 4/15 4/15 3/15 4/15
HEME-iron 3.7±0.3 4.2±0.4 4.1±0.2 4.1±0.2
Zinc mg 13.7±1.0 14.7±1.4 17.2±1.2 19.2±3.3
< 12 6/15 4/15 5/15 1/15
WBA: wheelchair basketball athletes; GAL: gym attendees with FM% below 17; GAH: gym attendees with FM% above 18; NSA: inactive men who do not practice sport activity.
RE: retinol equivalents. Continuous variables are expressed as means with SEM. Student-Newman-Keuls: multiple comparison (a) versus (b): p<0.05. Categorical variables, χ 2:
*p<0.05.

Table 5. ON and Med-D adherence.

Score WBA NSA GAL GAH


ORTO-15 36.9±1.1 34.7±1.1 37.4±1.0 37.3±0.5
ORTO-12 29.9±0.9 27.6±0.9 29.9±0.8 29.7±0.5
ORTO-11 27.2±0.9 25.8±0.8 27.5±0.8 27.8±0.6
ORTO-9 24.3±1.1 22.5±1.2 25.2±1.0 23.9±0.7
ORTO-7 19.2±0.8 18.3±0.5 19.7±0.4 20.4±0.5
ORTO-6 17.7±1.0 16.0±1.0 18.3±0.8 17.2±0.7
MDS 6.3±0.6 6.7±0.5 7.5 ± 0.5 7.6 ± 0.5
MEDScore 30.1±1.2 29.5±2.1 33.1±2.0 34.5±1.5
MDS-CO 2.3±0.4 2.6±0.3 3.2 ± 0.3 2.9 ± 0.3
MEDScore-CO 16.3±1.1 (a) 16 9±1.1 (a) 20.3±0.8 (b) 20.3±0.7 (b)
MDS-IC 0.7±0.1 0.7±0.1 0.8 ± 0.1 1.0 ± 0.2
MEDScore-IC 6.5±0.3 5.0±0.6 5.9±0.5 6.6±0.5
MDS-D 3.3±0.3 3.4±0.2 3.5 ± 0.2 3.7 ± 0.2
MEDScore-D 7.3±0.7 7.5±0.9 6.9±1.1 7.5 ± 0.8
WBA: wheelchair basketball athletes; GAL: gym attendees with FM% below 17; GAH: gym attendees with FM% above 18; NSA: inactive men who do not practice sport activity.
ORTO: score and sub-scores of orthorexia (*reverse scores: individuals with lower scores have more symptoms). Continuous variables are expressed as means with SEM. MEDS-
core and MDS: adherences to Mediterranean diet. Sub-scores CO: coherent, IC: incoherent, D: different. Data are expressed as means with SEM, Student-Newman-Keuls: (a) versus
(b) p<0.05.

(2/15) had vitamin B2 intake below the recommended val- No significant differences were found in ON (Table 5).
ues. On the other hand, the mean intakes of vitamin B6 and The mean MEDScore-CO, including fruits, vegetables
vitamin A were higher in WBA, compared to the other and legumes, was higher in the GAL and GAH groups com-
groups (Table 4).
Dietary Intakes and Food Habits Endocrine, Metabolic & Immune Disorders - Drug Targets, 2022, Vol. 22, No. 1 43

pared to the WBA and NSA groups (Table 5). The other tively). with ON behaviour had lower intake of vitamin C.
sub-scores were not different (Table 5). In the GAH group, ON was also associated with low intake
of vitamin E (versus: ORTO-15: -0.781, p<0.001;
Spearman correlations revealed that WBA with lower
ORTO-12: -0.713, p<0.01; ORTO-11: -0.723, p<0.001;
ORTO-15 and ORTO-12 had higher MEDScore (Table 6).
ORTO-9: -0.611, p<0-05 and ORTO-6: -0.535, p<0.05) and
MEDScore was related with ORTO-7 in GAH and NSA vitamin D versus: ORTO-15: -0.619, p<0.05; ORTO-12:
(Table 6). However, GAH and NSA with eating behavior of -0.639, p<0.01; ORTO-11: -0.566, p<0.05; ORTO-9: -0.525,
ON had more and less adherence to Med-D, respectively. p<0.05 and ORTO-6: -0.528, p<0.05).
Correlations revealed that NSA (ORTO-15 versus vita- MEDScore was correlated with NBD (0.508 p=0.05).
min C: -0.540, p<0.05) and GAH (ORTO-11 and ORTO-7 On the contrary, MEDScore was inversely related to
versus vitamin C: -0.646, p<0.01 and -0.560, p<0.05, respec- PROT-AN in NSA and GAL (Table 6).

Table 6. Spearman correlations among WBA and control groups.

WBA NSA GAL GAH


IWBF class vs NA NA NA
MEDScore -0.569* - - -
NBD -0.754*** - - -
FM% -0.627* - - -
ORTO-15 vs
MEDScore -0.539* NS NS NS
GERD 0.543* NA NA NA
SSI -0.732** NA NA NA
Fat % En -0.652** NS NS NS
CHO % En 0.517* NS NS NS
PROT-AN NS -0.619* NS NS
ORTO-12 vs
MEDScore -0.539* NS NS NS
GERD 0.559* NA NA NA
SSI -0.732** NA NA NA
Fat % En -0.678** NS NS NS
ORTO-11 vs
Fat % En -0.649** NS NS NS
CHO % En 0.511* NS NS NS
PROT-AN NS -0.669** NS NS
ORTO-9 vs
GERD 0.584* NA NA NA
Fat % En -0.596* NS NS NS
PROT-AN NS -0.688** NS NS
ORTO-7 vs
MEDScore NS 0.526* NS -0.628*
SSI -0.517* NA NA NA
Fat % En -0.514* NS NS NS
PROT-AN NS -0.530* NS NS
FM% NS NS 0.548* 0.546*
ORTO-6 vs
Fat % En -0.543* NS NS NS
PROT-AN/kg NS -0.512* NS NS
FM% NS NS NS 0.510*
PROT-AN vs
MEDScore NS -0.608* -0.643** NS
CHO/kg 0.654** NS NS -0.571*
En 0.793*** NS NS NS
FM% -0.571* NS NS -0.611*
PROT-VEG vs
CHO/kg 0.950*** NS NS NS
Fibre 0.575* NS NS NS
En 0.900*** NS NS NS
NS: not significant; NA: not applicable; FM%: percentage of fat mass; IWBF: International Wheelchair Basketball Federation; ORTO: score and sub-scores of orthorexia (reverse
scores); MEDScore: adherence to Mediterranean diet. NBD: neurogenic bowel dysfunction; GERD: gastroesophageal reflux disease; SSI: starvation symptoms inventory; En: energy
intake; CHO/kg: carbohydrates’ intake g/kg BM/d; PROT-AN: proteins from animal sources (g/kg BM/d); PROT-VEG: proteins from vegetable sources (g/kg BM/d). †p=0.051;
*p<0.05, **p<0.01, ***p<0.001.
44 Endocrine, Metabolic & Immune Disorders - Drug Targets, 2022, Vol. 22, No. 1 Toti et al.

On the other hand, only in WBA both PROT-AN and players of the Turkish National Wheelchair Women’s Bas-
PROT-VEG correlated with both CHO and En (Table 6). ketball Team (fibre intake 13.7-42.4g/d) only 36.4% met the
ON correlated with fat % En and CHO % En in WBA only required fibre intake according to the Recommended Dietary
(Table 6). Allowances (RDA) [37].
FM% was inversely related to PROT-AN in WBA and Despite the need for nutrition education in relation to
GAH, but to ON only in GAH (Table 6). Besides, WBA of consumption of whole grains, legumes, vegetables and
the lower IWBF class had more FM% and higher NBD whole fruits [11, 31, 37], a high-fibre diet has been shown to
(Table 6). Moreover, ON was related to GERD (Table 6), prolong constipation, increase colonic transit time and in-
which was related to NBD (-0.520, p<0.05) and SSI (-0.643, crease NBD score in SCI patients [38]. Consumption of
p<0.01). Being IWBF class, ORTO scores and GERD rev- about 15g/d of dietary fibre could be beneficial in managing
erse scores (lower scores correspond to higher impairment NBD in SCI, whereas an increase in fibre intake from 25g/d
or symptoms), WBA with eating behavior of ON had more to 31g/d may increase evacuation time [39]. Therefore, it
symptoms and adherence to Med-D. has been suggested that clinicians may recommend a low-fi-
bre diet [38]. NBD can cause significant pain and discom-
4. DISCUSSION fort and is a source of emotional distress, negatively impact-
In the present study, the mean FM% of the WBA (Table ing participation in social activities and travel [7]. It has
2) was lower than those of WBA of the Great Britain Men's been reported that some individuals with SCI coped with
Wheelchair Basketball World Class Performance Program changes in bowel function by limiting how much they ate,
(26.6% ± 6.5%) [27] and of Swiss Elite Wheelchair Athletes by skipping meals or by avoiding some foods [7].
practicing various sports (25.2 ± 9.5%) [28], within whom It has been suggested that, among the British wheelchair
basketball game players showed the highest fat-free mass games players, low fiber intake could be related to individu-
[28]. However FM% of WBA was higher than GAL group alized bowel management strategies [32]. Low consumption
and not significantly different from the other two control of fibre induces dysbiosis [12]. The latter has been found in
groups (Table 2). FM% was inversely related to ON in gym individuals with SCI [40, 41], particularly in those with bow-
atteendees and to IWBF class in WBA (Table 6). FM% was el dysfunction [42], where butyrate-producing bacteria were
inversely related to PROT-AN in WBA and GAH (Table 6). found to be specifically reduced compared to healthy con-
Differences in % of proteins from animal, vegetable and sup- trols [42]. Dysbiosis was related to serum lipids in individu-
plement sources were found among groups (Table 3). als with SCI [43, 44] and can lead to chronic low-grade in-
Mean intake of proteins, expressed as g/kg BM/d (Table flammation after SCI [12]. From that, personalized nutrition-
3), was in the range (1.2-1.7 g/kg BM/d) suggested for Para- al programs are recommended for wheelchair athletes with
lympic Athletes [29], however both lower and higher intakes SCI and NBD [12].
than those recommended were found in WBA, GAL and Bert et al. [45] observed that having a nutritional plan or
GAH (Table 3). Only in WBA both PRO-AN and PRO- nutritional restriction seems to relate to ON and pointed out
VEG intake correlated with both CHO and En (Table 6). that ON can have serious consequences on athletes’ health.
The observed CHO intake (Table 3) near to the lower In able-bodied gym members ON was associated with
limit of the recommendations (3.0–12.0 g/kg), was previous- uneasiness with body image and frequent exercising [3] and
ly reported in wheelchair athletes [30]. Similar results were to the use of dietary supplements [46].
found in male WBA of the Spanish National team [31] and
On the contrary, in WBA ON correlated with GERD and
CHO intakes resulted lower than those recommended for ath-
SSI (Table 6). A clear overlap exists between ON and eating
letes as previously reported in the British wheelchair games
disorders (ED) [5]. The “Australian Institute of Sport (AIS)
players [32]. An adequate CHO intake is essential to sustain
and National Eating Disorders Collaboration (NEDC) posi-
both general health and immune function [33, 34]. We in-
tion statement on disordered eating in high-performance
cluded AQUA among secondary outcomes for WBA, be-
sport” pointed out the importance of the early identification
cause clinical conditions of Paralympic athletes predispose
of ED and low energy availability in athletes [47]. Although
them to an increased risk of illness compared to able-bodied
the control of body composition may contribute to an in-
athletes [35], with a high incidence rate of respiratory sys-
creased prevalence of ED, body mass should not be the sole
tem illness, but also of the digestive tract [35, 36]. However,
focus of the multimodal assessment of ED and among risk
neither Med-D adherence nor ON were related to AQUA, as
factors there are chronic disease (including diabetes) and gas-
well as macronutrient intake.
trointestinal conditions [47]. The position statement suggest-
WBA and GAH with ON had higher adherence to Med- ed nutritional and body composition assessments, as well as
D, whereas NSA had less adherence to Med-D. However, education sessions and individualized nutritional interven-
MEDScore-CO was lower in WBA compared to GAH and tions [47]. In male elite WBA, the macronutrient distribu-
GAL. The MEDScore-CO includes fruits, vegetables and tion improved, after advice during a precompetitive-period,
legumes. Accordingly, Grams et al. [31] reported that from 3.8 ± 1.3 g/kg to 4.2 ± 1.9 g/kg CHO, from 1.7 ± 0.6
legumes were consumed in minimal amounts by WBA be- g/kg to 1.5 ± 0.5 g/kg protein, and from 36 ± 5% to 32 ± 5%
longing to the Spanish National Team. Moreover, among of En derived from fat [48].
Dietary Intakes and Food Habits Endocrine, Metabolic & Immune Disorders - Drug Targets, 2022, Vol. 22, No. 1 45

The adequacy of the micronutrient intake by elite male Although the world-class quality of the sample is among
WBA, belonging to the Spanish National Team, was posi- the strengths of this study, we will need to further explore
tively related to their total En and fruits and cereals were and confirm the relationship between gastrointestinal symp-
within the food groups found to be predictors of adequate in- toms and adherence to Med-D in a larger participant sample
take of most micronutrients [31]. In the present study many that includes women, varying types of Paralympic sports
volunteers did not meet the recommendations for some mi- and athletes from both the pre-elite and elite levels. Howev-
cronutrient (vitamin D, B1, B2, B12, C and calcium, Table er, among the elite British wheelchair games players, male
4), whereas iron intake was adequate in the majority of the showed significantly higher daily energy, CHO and protein
cases. Previously reported percentages of WBA who meet intakes than female, but En derived from CHO, protein, and
the requirements according to the RDA were 63.6%, 100%, fat were similar (53.6%, 16.9% and 29.3% for men and
72.7%, 81.8%, 95.5%, 86.4% and 27.3% for vitamin B1, 53.3%, 19.0% and 26.8% for women) [32].
B2, B12, C, D, calcium and iron, respectively [37].
CONCLUSION
It has been suggested that supplements may be a possi-
ble solution for WBA, if adequate micronutrient intake can- Although many volunteers in all groups did not follow
not be achieved through regular dietary intake alone [31]. Vi- the National recommendations, Paralympic athletes require
tamin D was among the commonly consumed supplements specific nutritional guidelines, considering their specific
by male rugby wheelchair athletes [49], whereas in our health conditions and possible related gastrointestinal symp-
study no WBA reported any vitamin D supplementation de- toms. Personalized dietary and supplementation strategies to
spite the low intake (Table 4). cover nutritional demand and support WBA health and
longevity should consider self-regulation of food choice of
In mice, low Vitamin D dietary intake induced a lower WBA, due to accumulated experience and exposure to vari-
microbial diversity, neuronal hyperexcitability and altered ous tolerated foods. In WBA, eating behaviors seem to be
nociception mediated by the endocannabinoid system at the due to self-control of gastrointestinal symptoms and commit-
spinal cord level [50]. In a study on osteoporotic patients ment to well-being (including ON and Med-D adherence)
with SCI, the supplementation with calcium, vitamin D and and could be a response to starvation symptoms. Our find-
omega-3 polyunsaturated fatty acids for 4 months, did not ings suggest that athletes’ opinions and experience in self-
change significantly pro-inflammatory cytokines [51]. management of health conditions related to their impairment
On the contrary, proinflammatory markers were negative- should be included in the design of an integrated approach
ly correlated with dietary intake of anti-inflammatory nutri- to tailored education and dietary interventions, in order to
ents, such as omega-3 fatty acids, vitamin A, carotenoids, improve both compliance and efficacy.
and zinc, in individuals with SCI following an anti-inflam-
matory diet for 3 months [52]. This anti-inflammatory diet LIST OF ABBREVIATIONS
excluding foods with high glycemic indices, common intoler-
ances (cow's milk), and foods that negatively influence car- AIS = Australian Institute of Sport
diovascular health such as hydrogenated oils; and introduc- ANOVA = Analysis of Variance
ing nutraceuticals with anti-inflammatory effects (omega-3,
chlorella, coenzyme Q10, n-acetyl-cysteine, mixed toco- AQUA = Allergy Questionnaire for Athletes
pherols, alpha lipoic acid, zinc, selenium, green tea extract, ASIA = American Spinal Injury Association Impair-
curcumin and a vegetable-based protein powder), reduced in- ment Scale
flammation [53, 54]. After this treatment, the decrease of in-
terleukin-2 and interferon-gamma correlated with the reduc- BM = Body Mass
tion of the sensory neuropathic pain [54]. CHO = Carbohydrates
AIS and NEDC found paucity of data in Paralympics, ED = Eating Disorders
with further research and understanding required in this pop-
ulation. En = Energy Intake
Therefore, the major strength of our study is that we FM% = Fat Mass Percentage
found that WBA had different eating habits compared to GAH = Gym Attendees with FM%>18
gym attendees or to people who do not practice any sport ac-
tivity. Another point of strength is the suggestion that ON in GAL = Gym Attendees with FM%<17
WBA is related more to physical rather than psychological GERD = GastroEsophageal Reflux Disease
factors. In particular, ON was inversely related to FM% and
correlated with SSI in GAH and WBA, respectively. IWBF = International Wheelchair Basketball Feder-
ation
The study has also several limitations. The major limita-
tion of our study is that the relatively limited sample size pre- L = Left
vented us from sub-grouping WBA with different types and
Lum = Lumbar
degree of severity of their impairment.
46 Endocrine, Metabolic & Immune Disorders - Drug Targets, 2022, Vol. 22, No. 1 Toti et al.

LARN = Livelli di Assunzione di Riferimento di Nu- CONSENT FOR PUBLICATION


trienti ed Energia Per la Popolazione A written informed consent was obtained from all partici-
Italiana pants involved in the study.
LLA = Lower Limb Amputation AVAILABILITY OF DATA AND MATERIALS
MDS = Mediterranean Diet Score The datasets generated and analysed during the current
Med-D = Mediterranean Diet study are not publicly available (individuals’ data availabili-
ty is restricted by the Ethics Committee) but are available
NBD = Neurogenic Bowel Dysfunction from the corresponding autor, [IP], on reasonable request.
NEDC = National Eating Disorders Collaboration
FUNDING
NSA = healthy Individuals who do not Practice
Sport Activity The study was supported by FIPIC (Federazione Italiana
Pallacanestro In Carrozzina) and Ministero della Difesa (Pro-
OHC = Other Health Conditions ject AMAMP 2019-2021).
ON = Orthorexia Nervosa
CONFLICT OF INTEREST
ORTO = Orthorexia Score Research was funded by Federazione Italiana Pallacane-
PRO-AN = Animal Protein Intake stro in Carrozzina (FIPIC, Rome, Italy) and by Progetto
AMAMP (Ministero della Difesa). M.B. and S.B. were col-
PROT-AN = Proteins from Animal Sources laborators of FIPIC. M.B. is the Federal Doctor and S.B. col-
PROT-SUP = Proteins From Supplements laborated only in the impairment level and relative IWBF
class assessment. However, the funders had no role in the de-
PROT-VEG = Proteins from Vegetable Sources sign of the study; analyses, or interpretation of data. The
R = Right other authors declare no conflict of interest.
RDA = Recommended Dietary Allowances ACKNOWLEDGEMENTS
SB = Spina Bifida The authors would like to thank the volunteers who
SCI = Spinal Cord Injury willingly participated in this study, Fernando Zappile and
Alessia Ferri, President and General Secretary of the FIPIC,
SEM = Standard Error Mean respectively, who sponsored the project on the Italian Nation-
SSI = Starvation Symptom Inventory al WB teams, Bianca Maria Mariani (FIPIC, Rome, Italy)
for the recruitment of the athletes and Roberta Peluso for the
T = Thoracic photograph used in the graphical abstract. The authors ac-
TF = Transfemoral knowledge Dr. Claudio Andrew Gobbi for the English revi-
sion of the manuscript.
TR = Transradial
TT = Transtibial REFERENCES

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