Association between dietary inflammatory index and musculoskeletal disorders in adults

This research investigated how the Dietary Inflammatory Index (DII) related to musculoskeletal issues in adults. It used a cross-sectional design with a sample of 3477 female and 3572 male participants aged 35 to 65 from the Ravansar Non-Communicable Diseases cohort study in western Iran. The DII is calculated from a Food Frequency Questionnaire (FFQ) to measure dietary intake. Musculoskeletal disorders including back pain, back pain/stiffness, joint pain, and joint pain/stiffness were evaluated by the RaNCD cohort study physician using a standard questionnaire. Logistic regression analysis examined the association between DII and musculoskeletal disorders. The findings demonstrated a positive association between higher DII scores and back pain/stiffness (OR 1.32, 95% CI 1.04–1.73, P = 0.047). Furthermore, DII displayed a significant association with a heightened odd to joint pain (OR 1.26, CI 1.10–1.46) when compared to those with lower DII scores (Q3 vs. Q1). After adjusting for cofounding factors, the Q3 DII quintile participants showed a 44% higher odd of experiencing joint pain/stiffness (OR 1.44, CI 1.01–2.05, P = 0.047). However, the study found no significant association between back pain and DII (P > 0.05). In conclusion, the research suggests that consuming a pro-inflammatory diet might be linked to developing musculoskeletal issues in adults.

musculoskeletal pain has garnered considerable attention 7 .There exists a significant corpus of evidence reinforcing the notion that dietary factors play a pivotal role in the modulation of inflammation and potentially facilitate the onset of musculoskeletal pathologies [8][9][10] .Therefore, it has become imperative to confront this matter by effectively managing inflammation via dietary interventions [8][9][10] .Specific nutritional components, such as fruits, vegetables, whole grains, and spices, have demonstrated anti-inflammatory effects due to their rich antioxidant and polyphenol content 11 .On the other hand, high consumption of animal proteins, fats, sugar, dairy products, and refined carbohydrates has been linked to increased inflammation 12 .Some nutritional studies have indicated that anti-inflammatory foods like nuts, tea, fish, olive oil, and vegetables reduce inflammation and less severe musculoskeletal pain 13,14 .Therefore, an anti-inflammatory diet could be valuable in managing musculoskeletal conditions 7,15 .
The dietary inflammatory index (DII) can evaluate the overall nutritional pattern to gain more comprehensive insights into the diet-disease association 11,13 .Investigating the association between the DII and musculoskeletal pain is of great importance as it sheds light on how diet can impact the musculoskeletal health of adults.Previous studies have focused on exploring the association between the DII and factors such as handgrip strength and body composition (including fat mass, fat-free mass, and percent body fat) 16,17 .Although studies on this topic are limited, the results of a recent study performed on 212 elderly individuals showed that higher DII score was positively associated with musculoskeletal pain 7 .However, this current study is pioneering in the Western region of Iran, as it examines the link between DII and various types of pain, such as back pain, back pain/stiffness, joint pain, and joint pain/stiffness, among the adult population.

Study population
The present study was conducted using a cross-sectional research design and drew upon data from the ongoing non-communicable diseases cohort study (RaNCD) in Kermanshah province, in Western Iran.The study was specifically focused on individuals of Kurdish descent and has been ongoing since 2014.A total of 10,047 adults, comprising both males and females aged between 35 and 65 years, were recruited to participate in the study.Notably, the RaNCD project is a constituent of the more extensive Prospective Epidemiological Research Studies in Iran (PERSIAN) study, which has been granted ethical approval by Iran's Ministry of Health and Medical Education.Interested readers may consult earlier publications to comprehensively understand the PERSIAN and RaNCD cohort studies 18,19 .All the participants included in the current investigation were drawn from the RaNCD study's baseline phase, constituting a sample size of 10,047 individuals.
After applying exclusion criteria, such as cardiovascular diseases, cancer, type 2 diabetes, hypertension, osteoporosis history, pregnancy, and incomplete information, the final sample size was reduced to 7049 participants (refer to Fig. 1).The data collection process involved face-to-face interactions at the RaNCD cohort site, where questionnaires, measurements, and tests were conducted and evaluated.

Assessment of other variable
Data concerning various demographic factors and lifestyle aspects, such as age, gender, socio-economic status, place of residence, smoking habits, and alcohol consumption, were collected using digital questionnaires administered by trained interviewers.To capture information on chronic diseases, medications, and the use of NSAIDs (aspirin, ibuprofen, naproxen, celecoxib, ketorolac, diclofenac, indomethacin, and piroxicam), a medical history questionnaire was employed.Physical activity levels were evaluated through the PERSIAN cohort questionnaire, and participants' responses were measured in terms of the metabolic equivalent of task per hour per day (MET/h per day), following a methodology from a separate study 19 .The collected MET values were categorized into three tertiles: Light (< 3), Moderate (3-6), and High (≥ 6) 20,21 .

Dietary inflammatory index (DII)
The DII score was computed for participants at the RaNCD study site through the completion of a 118-item Food Frequency Questionnaire (FFQ), which is known for its validity and reliability 22 .This questionnaire was based on the method developed by Shivappa et al. 23 and focused on 45 food items that have been shown to influence inflammation, either positively or negatively.For this particular study, our focus was on 31 distinct food items, including onion, garlic, coffee, tea, energy, protein, carbohydrates, fiber, and various essential vitamins (A, C, D, E, B1, B2, B3, B6, B12, and folate), as well as beta-carotene, total fat, saturated fatty acids (SFAs), monounsaturated fatty acids (MUFAs), polyunsaturated fatty acids (PUFAs), omega-3 and omega-6 fatty acids, cholesterol, magnesium, iron, selenium, and zinc.To determine the DII score, we compared the intake of these selected food items to global mean and standard deviation data obtained from 11 worldwide studies 23 .The cumulative sum of these specific food items was then used to calculate the DII score.A positive DII score indicated a pro-inflammatory diet, while a negative score suggested an anti-inflammatory diet 23,24 .For analysis, we further categorized the DII scores into quartiles, with the first and fourth quartiles representing the lowest and highest DII scores, respectively.

Outcomes
The RaNCD cohort study evaluated musculoskeletal conditions, encompassing a range of disorders like back pain.Back pain was defined as the experience of continuous back pain lasting over a week and significantly interfering with daily activities.Additionally, the study included back pain/stiffness, which referred to back pain accompanied by morning stiffness lasting an hour or more, as well as joint pain, indicating a history of experiencing pain in the joints.Moreover, standard pain/stiffness was also assessed, which reflected a history of joint pain and morning stiffness lasting an hour or more.To evaluate these conditions, physicians assessed the participants and asked specific questions to which the participants responded.
The questions asked were as follows:

Results
The study examined participant characteristics based on DII quartiles, as shown in Table 1.Various variables, such as age, gender, place of residence, job, socio-economic status, alcohol consumption, BMI, WHR, energy intake, protein, fat, fiber, zinc, calcium, Fe, B6, B12, and physical activity, exhibited significant differences (p < 0.001).The average DII quartiles ranged from − 4.03 ± 0.40 (Q1: indicating the most anti-inflammatory diet) to − 0.10 ± 1.06 (Q4: suggesting the most pro-inflammatory diet).Urban residents were predominantly found in Q4, demonstrating a significant difference in the DII quartiles (p < 0.001).Furthermore, 39.84% of participants who consumed alcohol were in the highest DII quartile (the most pro-inflammatory diet) (p < 0.001).
Participants with a higher socio-economic status also showed a notably higher DII (p < 0.001).The fourth quartile displayed a significantly higher average energy intake (3398 ± 971.78), protein (  1).

DII and back pain, back pain/stiffness, joint pain, and joint pain/stiffness
The study's results indicate that odds ratios are associated with back pain/stiffness and joint pain/stiffness concerning the DII quartiles.For back pain/stiffness, the odd was 1.32 times higher in the fourth DII quartile compared to the first quartile (OR 1.32, CI 1.04-1.73),and this association remained significant in models 2 and 3. Interestingly, no significant association was found between back pain and DII (p > 0.05).
Regarding joint pain, individuals in the third DII quartile had a 1.20 times higher odds ratio than the first.This association persisted after controlling for confounding variables in models 2 and 3 (OR 1.35, CI 1.17, 1.56; OR 1.26, CI 1.10-1.46,respectively).Additionally, the most pro-inflammatory diet in the fourth quartile showed a significant association with joint pain in model 2 (OR 1.30, CI 1.12-1.50).
After adjusting for confounding variables, the study found a direct association between DII and joint pain/ stiffness.In the third DII quartile, the odds ratio of joint pain/stiffness was 1.44 times higher than in the first quartile (OR 1.44, CI 1.01-2.05)(Table 2).

Discussion
The main outcome of this research is the presence of a direct relationship between the degree of dietary inflammation and back pain/stiffness and joint pain/stiffness, independent of potential confounders such as age, gender, BMI, energy intake, and physical activity levels.However, it is essential to mention that this relationship did not follow a dose-response pattern.
The relevant studies on this topic are scarce, and those which do exist are often on unhealthy population.The study conducted by Correa-Rodríguez et al. focused on menopausal women with fibromyalgia syndrome.It highlighted that the DII showed a significant association with increased pressure pain thresholds in some sites such as knee 24 .Another investigation by Toopchizadeh et al. involved 220 knee osteoarthritis patients and revealed a positive link between higher DII scores and increased pain levels based on the visual analog scale.They also have demonstrated a detrimental association between the DII scores and physical function and emotional well-being, independent of potential confounding variables such as age, gender, body mass index, and physical activity levels 25 .Moreover, Strath and colleagues have reported that the DII score was linked to the severity of movement-evoked pain in women afflicted with chronic back pain, although no such association was observed in men 26 .Similarly, the results of a recent study performed on 212 elderly individuals showed that grater DII score was positively associated with intense musculoskeletal pain 7 .Also, evidence shows that chronic low back pain may be related to lumbar vertebral bone mineral density (BMD) among community-dwelling middle-aged adults 27 .Although Cervo and colleagues observed a significant association between DII scores and lumbar spine BMD (B 0.013; 95% CI − 0.024 to − 0.002) in community-dwelling Australian older men, they didn't find this association in women 28 .Sakai and colleagues revealed that low back pain had a negative correlation with skeletal muscle mass rather than with BMD 29 .Furthermore, Eguchi, et al. and Kim, et al. reported that chronic low back pain was positively associated with sarcopenia 30,31 .Therefore, musculoskeletal disorders are greatly influenced by sarcopenia and muscle mass.Chen and colleagues found that adherence to diets with high DII scores is significantly associated with a lower muscle mass and strength and higher risk for sarcopenia in older US adults 32 .Esmaeily and colleagues showed that higher DII scores were significantly associated with higher odds of sarcopenia and lower handgrip strength in community-dwelling older subjects 33 .Taken together, a recent meta-analysis on 24 studies involving 56,536 participants revealed that high DII scores increase the odds of low skeletal muscle mass, low skeletal muscle strength, and sarcopenia 34 .
Epidemiological investigations consistently demonstrate that dietary patterns characterized by a low DII, denoting an anti-inflammatory dietary regimen, are linked with a diminished incidence of non-communicable chronic ailments featuring inflammatory etiologies.Prior research has additionally established a correlation between DII scores and the probability of developing Rheumatoid arthritis 35 and the quantity of tender and swollen joints present in individuals with this ailment 36 .Similarly, Sköldstam et al. found that adhering to a Mediterranean diet, known for its anti-inflammatory properties, was negatively associated with pain levels in patients with rheumatoid arthritis 37 .Specific dietary components like omega-3 polyunsaturated fatty acids 38 and polyphenols have also been shown promising effects in animal models' reduction of intervertebral disc degeneration 39 .Disc degeneration is the main cause of morning back stiffness and pain among healthy subjects 40 .
A possible mechanism of inflammation reduction by anti-inflammatory diet could be through the reduction of prostaglandins, interacting with neuromodulator pathways (gamma-aminobutyric acid receptor signaling), www.nature.com/scientificreports/inhibiting inflammatory signaling, focusing on l-arginine/nitric oxide signaling, and decreasing enzyme activity such as cyclooxygenase 2 7 .Chronic systemic inflammation can interrupt muscle homeostasis through suppressing insulin-like growth factor 1 (IGF-1) mediated by activation of the ubiquitin-proteasome system 41 .Also, elevated levels of inflammatory mediators such as interleukin 1-1β, tumor necrosis factor α, Interferon-γ in blood flow can lead to skeletal-muscle wasting through impairing the regenerative function of muscle stem cells and inducing accumulation of extracellular matrix and subsequently muscle fibrosis 42,43 .Hence, including anti-inflammatory factors in one's diet may be linked to a reduced risk of experiencing back pain and stiffness by lowering inflammation, minimizing intervertebral disc degeneration, altering pressure pain thresholds, and preventing skeletal-muscle weakness and wasting.
The key strength of this study lies in its utilization of data from a large population of a race and region.However, several limitations need to be acknowledged.Firstly, this research cannot reveal the causal relationship because of the nature of the cross-sectional study design, and it necessitates longitudinal studies to validate and establish the results conclusively.Secondly, the recall and self-reporting of outcomes in this study are vulnerable to information bias.Inaddition, people suffering from moderate to severe pain usually follow healthy dietary recommendations to reduce the symptoms of the disease.This phenomenon can affect and weaken the relationship between the dietary inflammatory index and pain.Thirdly, the absence of measurements for the origination and area of pain as well as the degree and intensity of pain hampers the interpretation of the findings.Furthermore, it is essential to note that the findings of this study cannot be readily applied to other populations due to specific factors.Notably, the participants in this study were highly active individuals engaged in physically demanding occupations such as farming and livestock farming, setting them apart from other groups.As a result, conducting further investigations while addressing the current study's limitations is highly recommended.

Conclusion
The findings of this study lead to the deduction that there exists a significant association between the inflammatory characteristics of the diet and higher risk of having back pain/stiffness, as well as arthralgia among the subjects under examination.Consequently, it is advisable to commence dietary interventions at an early stage for the benefit of grownups who experience musculoskeletal problems.

Figure 1 .
Figure 1.Flow diagram of the study participants.

Table 2 .
Crude and adjusted odds ratios (95% CIs) for musculoskeletal disorders across the quartiles of dietary inflammatory index (DII).Model 1 Crude, Model 2 Adjusted for age and gender, Model 3 Adjusted for age, gender, BMI, physical activity, energy intake and SES.