A close look at the nutritional status and mediterranean diet adherence in patients with behcet’s syndrome

Abstract

OBJECTIVE:

This study aimed to investigate Behçet’s syndrome (BS) patients’ regarding anthropometric measurements, daily energy and nutrient intake, and the MD adherence of patients.

METHODS:

100 consecutive patients with BS were prospectively enrolled in two rheumatology outpatient clinics. Mid Upper Arm circumference (MUAC), Triceps skinfold thickness (TST), Mid Upper Arm Muscle Circumference (MUAMC), and Mid Upper Arm Muscle Area (MUAMA) measurements of patients were compared with Turkish reference values. Participants’ daily energy and nutrient intake were categorized by the ‘MD Adherence Score.’

RESULTS:

Thirty patients (30%) had only mucocutaneous involvement. According to reference values, 47%, 36%, 14%, and 27% of the participants had low percentile values (<50. percentile) for MUAC, TST, MUAMC, and MUAMA, respectively. Walnuts (35%), eggplant (35%), and tomatoes (13%) were reported as the most prominent foods for symptom exacerbations. The mean MD adherence score was 23.5±6.5 (male: 23.2±6.9; female: 24.2±5.9) points and the adherence status was average (60%) and poor (35%) in the majority of the patients.

CONCLUSIONS:

Food consumption is important regarding symptom occurrence and multidisciplinary management of BS. Some participants had poor adherence to the MD. Increased waist/hip ratio, BMI, and decreased TST and MUAMA may indicate body muscle mass and unhealthy eating patterns. Patients with BS need encouragement for healthy eating habits.

Keywords

Behçet’s syndrome nutrition dietary habits disease activity mediterranean diet

1 Introduction

Behçet’s syndrome is a multisystem and vasculitic disorder of unknown etiology that causes mucocutaneous, musculoskeletal, ocular, vascular, neurologic, and gastrointestinal involvement [1], and it was first defined by Turkish dermatologist Prof. Hulusi Behçet, M.D. in 1937 [2]. BS is most commonly seen in countries known as the “Silk Road,” including Turkey [3]. There is no specific single laboratory test or biomarker to make the diagnosis, and well-known diagnostic or classification criteria can be helpful [4].

Inflammation is a physiological process involved in the defence of the body and the repair of tissues. Trauma, toxins, or allergic reactions can activate inflammation that stimulates the development of diseases such as cardiovascular disease, autoimmune disease, neurological disease, or cancer. Dietary composition (unrefined carbohydrate, fiber, fatty acid composition, magnesium, carotenoids, and flavonoids) affects some inflammatory markers (proinflammatory/anti-inflammatory cytokines) [5, 6]. Anthropometric measurement and weight management are significant for evaluating dietary sufficiency and controlling BS symptoms [3, 7].

Mediterranean Diet (MD) is characterized by a high intake of plant-based foods (polyphenols, fiber) and olive oil (monounsaturated fatty acids), moderate intake of fish (n-3 fatty acids) and poultry, and low consumption of meat, high-fat dairy products (lower saturated fatty acids intake) and sweets [8]. A beneficial effect of adherence to the MD is undoubtedly the reduction of mortality from all the causes, and it may become the diet of choice for diminishing chronic inflammation in clinical practice [9]. A higher adherence to the MD is associated with a lower risk of noncommunicable diseases due to its anti-inflammatory and antioxidative effects [10]. MD can decrease mortality risk and improve psychological well-being and perceived health status [9].

Management of BS, including medical therapies, nonmedical regulations, and lifestyle changes, requires detailed care by a multidisciplinary team [11]. The relationship between BS and nutrition has yet to be determined. However, diet-related factors and nutritional habits may be associated with pathogenesis and/or disease activity (oral ulcers) in some inflammatory conditions [12, 13]. Similarly, there has yet to be an apparent nutritional recommendation in international recommendations/guidelines for Behcet’s syndrome management [14]. Some guidelines for BS success only include “healthy eating,” but the healthy eating statement is not explained. This study aimed to investigate the dietary intake profile and MD adherence in patients with BS as well as study which foods may affect BS syndromes.

The hypotheses of this study are as follows:

MD adherence positively affects the anthropometric measurements of patients with BS.

Patients with high MD adherence have a higher intake of nutrients with beneficial health effects.

Some foods affect BS symptoms, especially oral ulcers.

2 Methods

2.1 Study population

One hundred consecutive patients with BS from Hacettepe University Vasculitis Research Centre, Ankara/Turkey, and the Rheumatology Clinic of Gülhane Training/Research Hospital, Ankara/Turkey, were included in the study between 1 November 2018 - 30 April 2020. All adult BS patients aged 18–60 years referred from Rheumatology clinics were included in the study. Patients with cancer (cachexia), dementia, or mental difficulties were excluded from the study. All study data were collected on the same day using a standard questionnaire by face-to-face interviews with dieticians.

Demographics and clinical features of patients were recorded. This study has been approved by the Local Ethics Commission, and all participants gave written informed consent. Since voluntariness was taken as a basis for participation, all the participants signed the volunteer consent form.

2.2 Anthropometric measurements

Anthropometric measurements were measured, such as weight, height, Mid Upper Arm circumference (MUAC, cm), waist (cm) and hip (cm) circumference, and Triceps skinfold thickness (TST, mm). The weight and height of the participants were measured with an electronic weighing scale sensitive up to 0.1 kg (Tanita BC 418MA, Tokyo, Japan). Mid Upper Arm circumference, waist, and Hip circumference were measured by tapeline. The Triceps skinfold thickness of the participants was measured with a caliper (Holtain, UK). Some patients did not want their waist measured, hip circumference, or TST, so these measurements were not evaluated.

Body Mass Index (BMI), Mid Upper Arm Muscle Circumference (MUAMC), and Mid Upper Arm Muscle Area (MUAMA) were calculated (BMI: Weight (kg)/ Height (m)²; MUA muscle circumference: MUAC (cm) - (π×TST); MUA muscle area: [[MUAC (cm) - (π×TST)]² / 4π]- 10 cm² (for male) or 6.5 cm² (for female). BMI, MUAMC, and MUAMA were evaluated by adult Turkish anthropometric references according to age and gender [15]. The evaluation was made according to percentile values and 50. percentile values were accepted as adequate.

2.3 Nutritional assessment and adherence to the mediterranean diet

The food consumption data was collected based on a 24 h-recall food consumption questionnaire using a photographic atlas of food portion sizes. Energy and nutrient intake were calculated by the BEBİS (Nutrition Data Base) software analysis system. Daily energy and nutrient intake were compared by Turkish references according to a 24-hour food consumption questionnaire [16, 17].

Mediterranean diet adherence was assessed by the Mediterranean Diet Index was developed in 2005 by Christos et al. [18]. In the MD index, food frequencies were categorized such as; “never,” “1–4 serving/monthly”, “5–8 serving/monthly”, “9–12 serving/monthly”, “13–18 serving/monthly” and “> 18 serving/monthly”. MD score was calculated for each patient according to reported food frequency consumption. MD adherence was deemed as poor (0–20 points), average (21–35 points), and good (36–55 points)(18–20).

The participants were assessed regarding the foods that can affect/cause BS symptoms. The questionnaire consisted of open-ended questions assessing which foods may affect BS syndromes. Subjects who answered questions such as “Do you believe the foods affect BS symptoms’?” and “Which food does affect BS symptoms’?”

2.4 Statistical analysis

Descriptive statistics of the data were expressed as mean, standard deviation, number, and percentages. Normality was tested by Shapiro-Wilk. Non-parametric data was analyzed. Mann Whitney U and Independent samples T-test was used for normal data analysis. All analyses were performed using SPSS (PASW) 23.0 software (SPSS Inc, Chicago, Illinois).

3 Results

Fifty-six (56%) patients were male. The mean age of BS patients was 38.5±10.9 years for males and 42.7±13.5 years for females. Thirty patients (30%) had only mucocutaneous involvement (male: 8.9%; female: 56.8%), and 70% of patients had organ involvement (male: 91.1%; female: 43.2%) (Table 1).

Table 1

Anthropometric measurements according to MD adherence and gender

Male									Female									Total
Anthropometric	Poor MD		Average MD		Good MD		p	Total		Poor MD		Average MD		Good MD		p	Total		p
measurements	adherence		adherence		adherence				adherence		adherence		adherence		Total
	n	$\bar{x}$ ±SD	n	$\bar{x}$ ±SD	n	$\bar{x}$ ±SD		n	$\bar{x}$ ±SD	n	$\bar{x}$ ±SD	n	$\bar{x}$ ±SD	n	$\bar{x}$ ±SD		n	$\bar{x}$ ±SD
Age (years)	23	38.2±10.3	30	38.7±11.9	3	38.0±7.8	0.945	56	38.5±10.9	12	52.0±11.6	30	39.0±13.0	2	42.0±4.2	0.018	44	42.7±13.5	0.089
Weight (kg)	23	74.5±11.8	29	75.2±13.6	3	75.6±7.0	0.972	55	75.0±12.4^a	12	71.1±9.2	30	68.1±13.9	2	54.1±1.0	0.120	44	68.3±12.8^b	0.01
Height (cm)	23	171.5±9.9	29	172.9±7.1	3	174.3±7.5	0.668	55	172.4±8.3^a	12	158.3±5.8	29	161.2±5.5	2	159.0±5.7	0.434	43	160.3±5.6^b	<0.01
Waist circumference (cm)	21	91.2±9.7	29	88.9±12.6	3	85.7±3.1	0.373	53	89.6±11.1	11	91.0±11.5	29	82.5±15.2	2	71.5±7.8	0.090	42	84.2±14.6	0.052
Hip circumference (cm)	21	98.9±7.2	29	97.3±8.7	3	95.3±6.1	0.263	53	97.8±7.9	11	104.3±5.6	29	101.4±12.3	2	91.0±1.4	0.068	42	101.7±10.9	0.179
Waist/hip ratio	21	0.9±0.1	29	0.9±0.1	3	0.9±0.0	0.645	53	0.9±0.1^a	11	0.9±0.1	29	0.8±0.1	2	0.8±0.1	0.111	42	0.8±0.1^b	<0.01
MUAC (cm)	21	29.4±3.1	29	27.9±3.5	3	29.5±1.3	0.265	53	28.6±3.3	11	30.4±3.5	29	28.1±4.3	2	26.0±0.0	0.184	42	28.6±4.1	0.973
Triceps skinfold thickness (mm)	17	12.0±4.9	17	15.3±14.6	1	11.0±0.0	0.951	35	13.5±10.7^a	11	28.0±8.4	23	22.8±7.8	2	20.9±1.0	0.168	36	24.3±8.0^b	<0.01
BMI (kg/m2)	21	25.6±4.5	29	25.1±4.1	3	24.8±0.2	0.639	53	25.3±4.1	12	28.5±4.2	29	26.0±6.1	2	21.4±1.1	0.093	43	26.5±5.7	0.257
MUAMC	17	28.9±3.0	17	28.2±3.4	1	30.2±0.0	0.821	35	28.6±3.1	11	29.5±3.4	23	27.9±3.9	2	25.3±0.0	0.187	36	28.2±3.7	0.666
MUAMA	17	53.9±14.7	17	52.8±16.9	1	62.4±0.0	0.922	35	53.6±15.5	11	59.4±18.0	23	54.7±17.2	2	44.7±0.1	0.403	36	55.6±17.0	0.605

^a,bNormality test shapiro-wilk; Non-parametric mann whitney U and Independent samples T test, p < 0.05. MUAC: Mid Upper Arm Circumference; BMI: Body Mass Index; MUAMC: Mid Upper Arm Muscle Circumference; MUAMA: Mid Upper Arm Muscle Area.

Demographics and anthropometric measurements of participants are shown in Table 1 according to group of MD adherence. Anthropometric measurements of patients were not different according to MD adherence groups (p > 0.05). The weight, height, and waist/hip ratio of males were higher than those of females (p < 0.05). The TST of males was lower than that of females (p < 0.05).

Forty-seven (47%), 36 (36%), 14 (14%), and 27 (27%) participants had low percentiles (< 50. percentile) values according to references for MUAC, TST, MUAMC, and MUAMA, respectively.

The MD score was negatively correlated with anthropometric measurements, such as waist circumference, hip circumference, MUAC, BMI, and MUAMC (p < 0.05) (Table 2).

Table 2

Correlation between Mediterranean Diet Score and anthropometric measurements obtained

Scores	Weight	Height	Waist	Hip	Waist/hip	MUAC	Triceps	BMI	MUAMC	MUAMA
	(kg)	(cm)	circumference	circumference	ratio	(cm)	skinfold	(kg/m2)
			(cm)	(cm)			thickness (mm)
Mediterranean	r	–0.191	0.015	–0.260^*	–0.217^*	–0.171	–0.263^*	–0.003	–.217^*	–0.252^*	–0.122
Diet Score	p	0.058	0.885	0.011	0.035	0.098	0.010	0.981	0.034	0.034	0.313
	n	99	98	95	95	95	95	71	96	71	71

**Correlation at 0.01(2-tailed), *Correlation at 0.05 (2-tailed), r: Correlation Co-efficient. MUAC: Mid Upper Arm Circumference; BMI: Body Mass Index; MUAMC: Mid Upper Arm Muscle Circumference; MUAMA: Mid Upper Arm Muscle Area; n: number of participants.

The mean MD scores were 23.5±6.5 points for all participants (male: 23.2±6.9; female:24.2±5.9). Patients with mucocutaneous involvement had a higher MD score (24.6±7.0 points) than patients with organ involvement (23.1±6.2 points), but this difference was not statistically significant (p > 0.05). There was no significant difference in MD scores according to sex (p > 0.05). Most participants’ MD adherence was evaluated as average (60%) and poor (35%).

The daily energy intake of males was 2016±591 kcal, and that of females was 1561±493 kcal. The protein intake for males averaged 67.8±24.4 g/day, while for females, it was slightly lower at 55.5±19.6 g/day. Interestingly, 47.2% of the protein intake for males was derived from vegetable sources, equating to 32.2±13.5 g/day. Similarly, 41.1% of females’ protein intake came from vegetables, amounting to 22.8(9.2 g/day). Daily omega-3 fatty acid and monounsaturated fatty acid (MUFA) intakes were 1.3±0.6 g and 27.7±11.6 g for males and 1.6±1.1 g and 24.9±10.0 g for females. Vitamin B₁₂ and folic acid intakes were 4.1±7.2 and 322.0±131.1 for males and 5.8±10.4 and 271.1±120.6 for females, respectively. Some important vitamin and mineral intakes of the participants are given in Table 3.

Table 3

Mediterranean Diet Adherence Score

Male		Female		Total
	n	$\bar{x}$ ±SD	n	$\bar{x}$ ±SD	n	$\bar{x}$ ±SD	p
Mediterranean diet score	56	23.1±6.9	44	24.1±5.9	100	23.5±6.5	0.360
Evaluation of Adherence	n	%	n	%	n	%
Poor MD adherence (0–20 points)	23	41.1	12	27.3	35	35.0
Average MD adherence (21–35 points)	30	53.6	30	68.2	60	60.0
Good MD adherence (36–55 points)	3	5.4	2	4.5	5	05.0

MD; Mediterranean diet.

Participants with higher MD adherence generally had higher energy and nutrient intakes. In particular, the energy, fiber, protein, vegetable protein, folic acid, iron, and zinc intake of participants increased with MD adherence (p < 0.05)(Table 4).

Table 4

Daily energy and nutrient intake according to MD adherence and gender

Energy and nutrient intake	Male			Female			Total
	Poor MD	Average MD	Good MD	Poor MD	Average MD	Good MD	Poor MD	Average MD	Good MD
	adherence	adherence	adherence	adherence	adherence	adherence	adherence	adherence	adherence
$\bar{x}$ ±SD	$\bar{x}$ ±SD	$\bar{x}$ ±SD	$\bar{x}$ ±SD	$\bar{x}$ ±SD	$\bar{x}$ ±SD	$\bar{x}$ ±SD	$\bar{x}$ ±SD	$\bar{x}$ ±SD		p
Energy (kcal)	1909±561.7	2103±638.9	1967±20.2	1645±604.2	1505±453.3	1881±395.6	1821±580.6^b	1809±627.7^b	1933±203.8^a	<0.01
Fiber (g)	16.2±6.9	23.5±12.8	22.6±6.4	15.3±6.2	16.1±7.4	26.2±1.5	15.9±6.6^b	19.8±11^b	24.1±5^a	0.044
Protein (g)	64±20.7	69.1±27.7	82±5.6	53.1±20.1	55.3±20	71.4±0.8	60.4±20.8^b	62.3±25^b	77.7±7^a	0.006
Vegetable protein (g)	30.9±14.5	33.1±13.8	33.2±1.5	23.4±9.6	22.1±9	30.4±11.1	28.3±13.3^b	27.6±12.8^b	32.1±5.8^a	<0.01
Fat (g)	78±28.1	83.8±33.6	105.6±18.9	76.8±29.6	69.4±23.1	94.8±21.7	77.6±28.2	76.7±29.6	101.3±18.2	0.085
Cholesterol (mg)	298±186.4	303.1±236.5	472.8±79.7	248.2±202.3	277.6±180.3	466.3±318.3	281.4±190.1	290.6±209.3	470.2±168.9	0.457
Omega-3 fatty acids (g)	1.2±0.6	1.4±0.6	1.6±0.3	1.5±1.3	1.6±1.1	2.3±1.6	1.3±0.9	1.5±0.9	1.9±0.9	0.637
Monounsaturated fatty acids (MUFA)(g)	25.5±9.3	28.4±12.4	37.1±17.4	25±10.1	23.5±9.2	42.9±0.1	25.3±9.4	26±11.1	39.4±12.7	0.213
Retinol (μg)	335.3±124.4	400.5±239	9289±15193.6	1579.7±3917.8	1336.7±3881.7	378.7±237.6	750.1±2271.9	860.4±2741.6	5724.9±11800.6	0.752
Vitamin D (μg)	1.3±1.1	1.3±1.4	2.7±0.8	1±1.4	2.1±5.5	3±3	1.2±1.2	1.7±3.9	2.8±1.6	0.545
Vitamin B₆ (mg)	1±0.3	1.2±0.6	1.6±0.6	1.1±0.5	1.1±0.5	1.6±0	1±0.4	1.2±0.5	1.6±0.5	0.583
Vitamin B₁₂ (μg)	2.8±1.3	3.2±2.2	21.6±28.5	7.1±14.7	5.4±9	3.9±1.3	4.2±8.5	4.3±6.5	14.5±22.4	0.931
Folic acid (μg)	268.7±93.5	346.1±128.3	479.6±236.3	268.8±101.8	265.4±130.3	363.1±45.4	268.7±94.7^b	306.5±134.4^b	433±180.3^a	0.018
Vitamin C (mg)	71.7±113.2	87.7±61.8	151.2±122.3	81.8±62.4	82.8±66.7	169.7±25.7	75.1±98.2	85.3±63.7	158.6±88	0.400
Calcium (mg)	494.1±177.2	700.3±294.1	859.9±334.1	597.5±280.4	578.8±199.8	640±176.6	528.6±218.2	640.6±257.4	772±279.5	0.668
Magnesium (mg)	218.6±103	270.9±129.4	375.7±65.1	201.5±110.5	206.4±83.4	359.7±111.6	212.9±104.2	239.2±113.1	369.3±72.8	0.070
Iron (mg)	10±3.4	12.3±4.5	18.3±9.6	8.8±4.5	9.2±3.5	15.8±3.5	9.6±3.7^b	10.8±4.3^b	17.3±7.2^a	0.006
Zinc (mg)	8.6±2.1	10.7±4.1	14.8±1.7	7.7±3.5	7.8±2.2	9.9±0.4	8.3±2.6^b	9.3±3.6^b	12.9±2.9^a	0.004

^a,bNormality test shapiro-wilk, Non-parametric mann whitney U, Independent samples T test, p < 0.05.

Forty participants (35.7% male; 45.5% female) believed that nutrition status might affect BS-related symptoms. Walnuts (35%), eggplant (35%), and tomatoes (13%) are reported as the most negatively effective foods on oral symptoms of BS. On the other hand, salted, hot, and acidic foods are effective on oral ulcers.

Discussion

Behçet syndrome is a multigenetic inflammatory systemic disorder that should be treated with a multidisciplinary health group. There is no effective nutritional therapy for symptoms of BS. However, successful management of food consumption in patients with BS should induce and maintain remission and improve patients’ quality of life. To the best of our knowledge, this is the first preliminary study to assess food consumption habits by point of MD compatibility and anthropometry in patients with BS. On the other hand, some foods, such as walnuts (35%), eggplant (35%), and tomatoes (13%), affect BS symptoms.

Anthropometric measurements are essential for evaluating the long-term nutrition status of patients with BS. According to World Health Organization anthropometric references for adults [7], participants’ mean waist/hip ratio and BMI value range from normal weight to pre-obesity level. Patients with BS have a low chronic illness risk regarding weight management, such as diabetes, cancer, and cardiovascular disease. Weight management is a significant indicator of energy balance when energy intake is sufficient. Lean body mass is evaluated by long-term protein intake and physical fitness [21]. Anthropometric measurements correlate with energy and protein intake (especially animal protein-essential amino acids). The participants’ daily energy and protein intake was sufficient. Animal protein intake in adults should be ¼ of the total protein intake, and vegetable protein intake should be ¾ [17]. In this study, participants’ protein intake was sufficiently met from animal sources (∼½); therefore, sufficient animal protein intake is important for the immune system [22]. Although the pathogenesis of BS is unclear, the immune system can play an important role in the development and progression of BS, and related factors include infection-related trigger factors, including antigens and autoantigens [29]. They will change if energy and protein consumption is consistently above and below the physiological needs for weight and/or lean body mass [22]. This study measured and evaluated MUAC, TST, MUAMC, and MUAMA for insufficient nutrition according to references. Forty-seven (47%), 36 (36%), 14 (14%), and 27 (27%) participants had low percentiles (< 50. percentile) values according to references for MUAC, TST, MUAMC, and MUAMA, respectively. The participants had a risk for MUAC. Medication usage (especially corticosteroids) and inflammation of BS have adverse effects on weight and lean body mass; therefore, BS’s sufficient energy and protein intake should be monitored and supported when needed. In particular, neurologic and vascular involvement or visual problems of BS can affect the physical activity status of patients because of immobilization. Patients with BS should be more physically active and perform physical resistance and aerobic exercises to improve their lean body mass.

The MD score was negatively correlated with waist circumference, hip circumference, MUAC, BMI, and MUAMC measurements in BS patients. An increase in the MD score was caused by waist circumference, hip circumference, MUAC, BMI, and MUAMC decline. Waist circumference, hip circumference, MUAC, and BMI are related to obesity, which should affect BS treatment. Higher MD scores were associated with lower micronutrient inadequacy. The MD pattern (extra virgin olive oil, nuts, red wine, vegetables, fruits, legumes, and whole-grain cereals) should positively affect obesity and weight control in humans [31, 32]. From this perspective, an increase in MD scores can improve the anthropometric measurements of BS patients.

Diet perspective and nutritional status are essential not only for the occurrence of symptoms but also for the efficient management of disease [1]. Erdogan et al., in their study of 74 patients with BS without neurological involvement and 72 patients with Neuro-BS studies, showed that malnutrition was higher in patients with Neuro-BS. Malnutrition was defined as a risk factor for a higher disability level and progressive disease course [23]. The daily fat intake of participants was very high; on the other hand, MUFA intake was insufficient. Fat intake may not be related to the development/progression of BS, but extremely high fat intake affects the oxidation of fatty acids and can cause some chronic diseases, such as diabetes and cancer [21]. In this study, the calcium intake of patient BS was insufficient for males and females according to reference values [17]. The daily calcium intake of males and females should be 1000–1200 mg, while 625.2±275.1 and 586.8±218.2 mg) were taken, respectively. Daily dietary vitamin D intake was 1.4±1.3 and 1.9±4.6μg, which were insufficient according to references [17]. The main vitamin D source is sunlight, so dietary vitamin D intake is not a valid value for evaluating body hydroxyvitamin D levels [30]. Serum hydroxyvitamin D levels were not assessed in this study, but Karatay et al. showed that serum 25-hydroxyvitamin D levels are decreased in patients with Behçet’s Disease [24]. Considering that calcium intake is insufficient, they should be more sensitive to bone disease and malformation. BS patients who use corticosteroids can be at risk for osteoporosis. Patients with BS should increase dairy and product consumption. Male BS patients’ magnesium intake is 255.4 mg/day, which is insufficient for males according to reference values (400–420 mg/day) [17]. Insufficient magnesium intake is associated with higher rates of diseases such as diabetes, cardiovascular disease, and bone malformation [25]. According to references, the daily iron intake of females is inadequate [17]. Iron deficiency prevents ulcer healing induced by BS. Patients with BS should be encouraged to consume iron sources such as meat, meat products, and dark green leafy vegetables. If BS has a biochemical indication for iron deficiency anemia, iron supplementation can be used by clinicians. Regular nutritional assessment is important for managing the disease and increasing the quality of life of patients with BS. In particular, oral ulcers and/or gastrointestinal system involvement can affect patients’ food consumption, nutrient bioavailability, and nutrition status.

Mucocutaneous features are the most common symptoms of BS disease; eye, vascular, and neurological involvement are the most serious [2]. There is no literature about the relationship between BS-related symptoms and food intake. Our most striking finding was discovering effective foods with BS-related symptoms. In this study, 40 participants (35.7% male; 45.5% female) believed that nutrition status might affect BS-related symptoms. Walnuts (35%), eggplant (35%), and tomatoes (13%) are reported as the most negatively effective foods on oral symptoms of BS. On the other hand, salted, hot, and acidic foods may increase mouth ulcers. This result was based on the patient’s belief, so there is a need for objective analysis. There is a need for more studies that discover effective foods for BS symptoms (especially oral ulcers) or irritable foods for BS involvement.

The MD is characterized by a high intake of plant-based foods (polyphenols, fiber) and olive oil (MUFA), moderate intake of fish (n-3 fatty acids) and poultry, and low consumption of meat, high-fat dairy products (lower saturated fatty acids intake) and sweets [8]. A high MD score is associated with a lower risk of noncommunicable diseases due to its anti-inflammatory and antioxidant effects [10]. The mean MD scores were 23.5±6.5 points for all participants (male: 23.2±6.9; female:24.2±5.9). Most participants’ MD adherence was evaluated as average (60%) and poor (35%). Daily omega-3 fatty acid and monounsaturated fatty acid (MUFA) intakes were 1.3±0.6 g and 27.7±11.6 g for males and 1.6±1.1 g and 24.9±10.0 g for females, respectively. Patients with BS need to increase their fruits and vegetables, fish (twice a week), nuts, legumes, and whole cereals. Our results were consistent with the MAMBA study results; MD supplemented with butyrate could restore immune system homeostasis and greatly impact cost sustainability for treating such a chronic and disabling inflammatory condition [26]. Some studies have shown that MD adherence is associated with a lower likelihood of developing some rheumatologic diseases, such as Sjögren’s syndrome and rheumatoid arthritis [27, 28]. We thought that the MD would slow down the inflammatory processes of BS disease.

This was the first study to assess the food consumption and anthropometry of patients with BS according to the MD and present the foods that probably affect BS symptoms. BS patients participated from two clinics; however, heterogeneity of the disease and exclusion of therapy of disease were limitations of this study. The other limitation of the study is that a non-validated questionnaire was used to assess the patient’s beliefs about BS symptoms. It is possible to say that MD is the most appropriate diet model for the management of the inflammatory process of BS. Nutritional assessment of BS patients is essential for integrative therapy.

In conclusion, most participants’ MD adherence was evaluated as average (60%) and poor (35%). The patients should be encouraged to consume more legumes, vegetables, and fruit. The other significant part of a healthy/quality life is weight management, so weight, BMI, waist/hip ratio, and body muscle mass should be followed by clinicians. On the other hand, patients with oral ulcers frequently should avoid walnuts, eggplant, and tomatoes.

Footnotes

Acknowledgment

The authors thank all participants who took part in this study.

Sources of support

The authors received no specific funding for this work.

Ethical consideration

Local Ethics Commission of Ankara Gülhane Training and Research Hospital (Approval number:18/324).

Author contributions

Nesli Ersoy, Ertuğrul Çağri Bölek, Bayram Farisoğullarí, Nur Çínar, Seda Çolak, Emre Tekgöz: inclusion of participants in the study.

Nesli Ersoy, Ertuğrul Çağri Bölek, Gökçen Garipoğlu, Sedat Yílmaz, Ömer Karadağ, Taner Özgürtaş: Conceptualization, Methodology, Resources, and Writing - Review & Editing, Supervision.

Nesli Ersoy, Ertuğrul Çağri Bölek, Sedat Yílmaz, Ömer Karadağ, Taner Özgürtaş: Project administration, Investigation, Formal analysis, Writing - Original Draft, and Visualization.

Declaration of competing interest

The authors declare no conflict of interest regarding financial and individuals.

Data availability statements

The datasets generated during and analyzed during the current study are available from the corresponding author on reasonable request.

References

Jennette

, Falk

, Bacon

, Basu

, Cid

, Ferrario

,et al. 2012 revised International Chapel Hill Consensus Conference Nomenclature of Vasculitides. Arthritis Rheum. 2013;65(1):1–11. doi: 10.1002/art.37715.

Behçet

. Über rezidivierende, aphtöse, durch ein Virus verursachte Geschwüre am Mund, am Augeund an den Genitalien. Dermatologische Wochenschrift. 1937;105, 1152–63.

Bettiol

, Prisco

, Emmi

. Behçet: the syndrome, Rheumatology.2020;59(3):101–107. doi: 10.1093/rheumatology/kez626.

The International Criteria for Behçet’s Disease (ICBD): a collaborative study of 27 countrieson the sensitivity and specificity of the new criteria. J Eur AcadDermatol Venereol. 2014;28(3):338–47. doi: 10.1111/jdv.12107.

Galland

. Diet and inflammation. Nutr Clin Pract. 2010;25(6):634–40. doi: 10.1177/0884533610385703.

Stromsnes

, Correas

, Jenny Lehmann

, Gambini

, Olaso-Gonzalez

. Anti-Inflammatory Properties of Diet: Role in Healthy Aging. Biomedicines. 2021;9(8):922. doi: 10.3390/biomedicines9080922.

WHO, Anthropometric Measurement. https://www. euro.who.int/en/health-topics/disease-prevention/zutrition/a-healthy-lifestyle/body-mass-index-bmi.Access: 17.07.2021.

Sofi

, Cesari

, Abbate

, Gensini

, Casin

. Adherence to Mediterranean diet and health status: meta-analysis. BMJ. 2008;11(337):1344. doi: 10.1136/bmj.a1344.

Sofi

, Macchi

, Abbate

, Gensini

, Casini

. Adherence to Mediterranean diet and health status: meta-analysis.. BMJ. 2013;39(4):335–42. doi:10.1002/biof.1096.

10.

Aridi

, Jacqueline

, Eugeni Roura

, Wright

ORL

. Adherence to the Mediterranean Diet and Chronic Disease in Australia: National Nutrition and Physical Activity Survey Analysis. Nutrients. 2020;12(5):1251. doi: 10.3390/nu12051251.

11.

Karadag

, Bolek

. Management of Behcet’s syndrome. Rheumatology. 2020;59(3):108–117. doi: 10.1093/rheumatology/keaa086.

12.

Giugliano

, Ceriello

, Esposito

. The effects of diet on inflammation: emphasis on the metabolic syndrome. J Am Coll Cardiol. 2006;48(4):677–85. doi: 10.1016/j.jacc.2006.03.052.

13.

Volle

, Fraison

, Gobert

, Goulenok

, Dhote

, Fain

,et al. Dietary and Nondietary Triggers of Oral Ulcer Recurrences inBehçet’s Disease. Arthritis Care Res (Hoboken). 2017;69(9):1429–1436. doi: 10.1002/acr.23155.

14.

Hatemi

, Christensen

, Bang

. 2018 update of the EULAR recommendations for the management of Behçet’s syndrome. Ann Rheum Dis. 2018;77(6):808–818. doi: 10.1136/annrheumdis-2018-213225.

15.

Pekcan

Determination of nutrition status. In: Baysal A, editor. Dietary hand book. 5. edition. Hatipoglu publisher; 2008. p. 67-143.

16.

Rakícíoglu

, Tek Acar

, Ayaz

, Pekcan

Meal and Food photography catalog. 3. edition. Ankara, Ata Ofset publisher; 2012.

17.

Hacettepe University, Faculty of Health Science, Department of Nutrition and Dietetics publication, Food and Dietary Guideline forTurkey. Ankara, July 2015.

18.

Pitsavos

, Panagiotakos

, Tzima

, Chrysohoou

, Economou

, Zampelas

, et al. Adherence to the Mediterranean diet is associated with total antioxidant capacity in healthy adults: the ATTICA study. Am J Clin Nutr. 2005;82(3):694–9. doi: 10.1093/ajcn.82.3.694.

19.

Katsouyanni

, Rimm

, Gnardellis

, Trichopoulos

, Polychronopoulos

, Trichopoulou

. Reproducibility and relative validity of an extensive semi-quantitative food frequency questionnaire using dietary records and biochemical markers among Greek schoolteachers. Int J Epidemiol. 1997;26(suppl):S118–27. doi: 10.1093/ije/26.suppl_1.s118.

20.

Supreme Scientific Health Council, Ministry of Health andWelfare of Greece. Dietary guidelines for adults in Greece. Arch of Hellenic Med. 1999;16, 516–24.

21.

Eaton-Evans

Nutrition Assessment: Anthropometry. Encyclopedia of human Nutrition. 3rd Editon 2013, 227-232.

22.

Mahan

, Raymond

(2017) Krause’s Food ’ the Nutrition Care Process (14.baskí). Washington: Elseiver.

23.

Erdogan

, Sorgun

, Kuzu Mumcu

, Kural

, Rzayev

, Yücesan

. Nutritional status in patients with neuro-Behcçet’s disease. Turk J Med Sci. 2021;51. doi: 10.3906/sag-2009-235.

24.

Karatay

, Yildirim

, Karakuzu

, Kiziltunc

, Engin

, Bavli Eren

, et alVitamin D status in patients with Behcet’s Disease. Clinics. (Sao Paulo). 2011;66(5):721–3. doi: 10.1590/s1807-59322011000500002.

25.

Mann

, Truswell

. (2007) Essentials of Human Nutrition. Oxford University Press.

26.

Pagliai

, Dinu

, Fiorillo

, Becatti

, Turroni

, Emmi

, Sofi

Modulation of gut microbiota through nutritional interventions inBehçet’s syndrome patients (the MAMBA study): study protocol fora randomized controlled trial. Trials. 2020;21:511. doi: 10.1186/s13063-020-04444-6.

27.

Machowicz

, Hall

, de Pablo

, Rauz

, Richards

, Higham

, et al. Mediterranean diet and risk of Sjögren’s syndrome. Clin Exp Rheumatol. 2020;126(4): 216–221.

28.

Diamanti

, Panebianco

, Salerno

, Di Rosa

, Salemi

, Sorgi

, et al. Affiliations expand. Impact of Mediterranean Diet on Disease Activity and Gut Microbiota Composition of Rheumatoid Arthritis Patients. Microorganisms. 2020;8(12)1989:doi:10.1016/s2665-9913(20)30064-3.

29.

Tong

, Liu

, Xiao

, Su

. Immunopathogenesis of Behcet’s Disease. Front Immunol. 2019;10:665. doi: 10.3389/fimmu.2019.00665.

30.

Jakobsen

, Wreford Andersen

, Christensen

, Andersen

, Bügel

. Vitamin D Vitamers Affect Vitamin D Status Differently in Young Healthy Males. Nutrients. 2018;10(1):12. doi: 10.3390/nu10010012.

31.

Castro-Barquero

, Lamuela-Raventós

, Doménech

, Estruch

. Relationship between Mediterranean Dietary Polyphenol Intake andObesity. Nutrients. 2018;17;10(10):1523. doi:10.3390/nu10101523.

32.

Ojeda-Rodríguez

, Zazpe

, Morell-Azanza

, Chueca

, Azcona-Sanjulian

, Marti

. Improved Diet Quality and NutrientAdequacy in Children and Adolescents with Abdominal Obesity after aLifestyle Intervention. Nutrients. 2018;13;10(10):1500. doi:10.3390/nu1010150.