WITHDRAWN: A Cross-sectional Study on Pelvic Inflammatory Disease Prevalence and Dietary Phosphorus using NHANES Data from 2015-2018

doi:10.21203/rs.3.rs-4414585/v1

Background
Phosphorus, an essential constituent of the human body, not only is present in human tissues but also actively participates in numerous metabolic processes. Pelvic inflammatory disease (PID), a condition that is widely observed in women and is considered to be a common problem in the field of gynecology, involves inflammation of female pelvic reproductive organs such as the uterus, fallopian tube, and ovary, along with the surrounding connective tissue and peritoneum. The objective of this study was to examine how dietary phosphorus intake is related to the prevalence of PID.

Methods
The female participants included in our cross-sectional investigation were sourced from the National Health and Nutrition Examination Survey (NHANES) spanning the years 2015 to 2018. Various statistical methods, such as regression equations with multiple factors, analyses within subgroups, and smooth curve fitting were utilized to analyze the relationship between dietary phosphorus intake and PID incidence.

Results
A decrease in PID incidence is associated with increased dietary phosphorus intake. Model 1, adjusted for age and ethnicity, exhibited a strong connection between dietary phosphorus consumption and PID (OR = 0.9995, 95% CI = 0.9992-0.9998, p = 0.002655), a finding further supported by Model 2, which underwent full adjustments (OR = 0.9996, 95% CI = 0.9993-0.9999, p = 0.011260). Moreover, a notable pattern toward a negative correlation between phosphorus intake and PID was observed in the tertile subgroups (OR < 1, p < 0.05), indicating a robust association. Additionally, the smoothed curves revealed a consistent link between PID and dietary phosphorus consumption.

Conclusions

The incidence of PID was found to be negatively linked to dietary phosphorus intake in this cross-sectional study. Nonetheless, additional prospective studies are required to confirm a direct link between dietary phosphorus and PID, bearing in mind the limitations of the current study.

pelvic inflammatory disease (PID)

phosphorus

diet

cross-sectional study

NHANES

Pelvic inflammatory disease (PID) is a commonly encountered gynecological ailment that affects a significant number of women. It involves inflammation of female pelvic reproductive organs, such as the uterus, fallopian tube, and ovary, along with the surrounding connective tissue and peritoneum. Bacterial infection of the upper reproductive tract primarily causes this condition.¹ It can be classified into two types: acute pelvic inflammatory disease and chronic pelvic inflammatory disease. Chronic pelvic inflammatory disease often persists due to incomplete resolution of acute pelvic inflammatory disease. The typical clinical manifestations of PID include persistent lower abdominal pain, which may manifest as a dull ache, sharp pain, or lumbosacral soreness. Additionally, patients may experience increased leucorrhea accompanied by odor and menstrual cycle changes, such as increased menstrual volume and prolonged menstrual disorders. When left untreated, PID can lead to several long-term complications, such as tubal infertility, chronic pelvic pain, and ectopic pregnancy. ²

Globally, PID is a significant contributor to health issues and mortality among women. The prevalence of PID varies significantly between regions, ranging from 0.28–1.67%³. Furthermore, other studies have estimated that PID affects between 4% and 12% of women of reproductive age worldwide¹ In the United States specifically, PID is estimated to affect 4.4% of the population, accounting for approximately 2.5 million cases⁴. The etiological factors of PID are diverse and complex, and include various factors including race, age, and smoking status⁵. The burden of PID varies among different demographic groups; for instance, black and non-Hispanic women and those residing in southern regions exhibit a higher prevalence, while young individuals and individuals of African or Caucasian descent are particularly susceptible². Additionally, a close correlation exists between PID and sexually transmitted infections (STIs). In economically developed countries, the proportion of individuals with PID attributed to sexually transmitted infections is estimated to reach 40%⁶. Regarding specific etiological factors, up to 85% of PID cases are attributed to sexually transmitted pathogens or pathogens associated with BV. In contrast, only 15% of acute pelvic inflammatory disease cases stem from bacterial colonization of the lower reproductive tract rather than sexual transmission⁷.

If PID is not promptly and effectively controlled, it may result in complications such as menstrual disorders, ectopic pregnancy, and infertility due to persistent infection, thereby exerting long-term negative effects on women's physical and mental health. Pelvic inflammatory diseases are caused by various mechanisms, including Chlamydia trachomatis, Neisseria gonorrhea and bacterial vaginosis-associated microorganisms, but there is no direct evidence that BV can independently cause pelvic inflammatory diseases^{8, 9}. Women face a greater risk of PID because they spend more time at home than men do¹⁰. While antibiotics are frequently employed in the treatment of pelvic inflammatory disease, this approach may not consistently yield optimal outcomes¹¹.

Due to the challenges associated with screening methods and an incomplete understanding of the epidemiological trends of pelvic inflammatory disease (PID) in various regions, research on the occurrence of PID in different areas is limited^{12, 13}. Hence, investigating the risk factors and treatment modalities for pelvic inflammatory disease is imperative. For patients diagnosed with pelvic inflammatory disease, early identification, prompt intervention, and timely treatment are essential to prevent further worsening of the condition.

Phosphorus is one of the indispensable elements within the human body, closely behind calcium in importance and ranking sixth among vital elements, after oxygen, carbon, hydrogen, and nitrogen. Phosphorus not only constitutes a component of human tissues, but also actively engages in numerous metabolic processes within the body. This essential nutrient plays a crucial role in various biochemical processes, including glycolysis, gluconeogenesis, energy metabolism, bone mineralization, cell signal transduction, and the regulation of acid-base balance across all cells of the body¹⁴.

Dietary phosphorus pertains to the phosphorus intake derived from food sources. This intake encompasses a broad spectrum of sources. Research indicates that among American adults, dietary phosphorus intake primarily originates from sources such as meat, dairy products, grains, and other food items ¹⁵. To maintain optimal health, adults require a moderate daily intake of phosphorus, as both excessive and insufficient amounts can lead to adverse health outcomes. Typically, a well-rounded diet can supply an adequate amount of phosphorus without necessitating supplementary intake. However, in certain situations, such as particular medical conditions or specific nutritional requirements, adjustments to phosphorus intake may be warranted. Phosphorus is a ubiquitous element in minerals, and dietary phosphorus serves as the primary source of serum phosphorus¹⁶. Moreover, there is a positive correlation between the amount of phosphorus absorbed by the intestine and its intake within a certain range. Specifically, as intake increases, the absorption of phosphorus by the intestine also increases¹⁷. In recent years, numerous scientific studies have highlighted that elevated serum phosphorus levels and increased phosphorus intake through diet substantially increase the risk of various health conditions, including cardiovascular diseases, kidney diseases, hypertension, diabetes, metabolic syndrome, and other related ailments. Additionally, elevated serum phosphorus levels and increased dietary phosphorus intake have been associated with an increased risk of all-cause mortality^18–21. Various research findings have revealed the intimate link between dietary phosphorus intake and a range of health disorders. A review by Kellar, K. et al. revealed that inadequate calcium and phosphorus intake during pregnancy and infancy (perinatal) increases the risk of metabolic bone disease (MBD), a condition characterized by reduced bone mass, abnormal bone mineral deposition, and an elevated fracture risk, particularly among preterm infants²². In contrast, Chavarro, J. E. et al. investigated the relationship between the consumption of fat, lactose, calcium, phosphorus, and vitamin D in dairy products and anovulatory infertility. After adjusting for other potentially confounding factors, they discovered that only dairy fat intake exhibited an association with a decreased risk of anovulatory infertility, whereas the intake of lactose and phosphorus did not demonstrate significant associations²³. Zhu, G. et al. reported that consuming more phosphorus through the diet was linked to a reduced likelihood of developing cervical cancer. They suggested that phosphorus might exert a protective effect against both cervical and endometrial cancer²⁴. Moreover, scientific evidence suggests that including dietary phosphorus in one's daily intake can play a crucial role in protecting against the development of cervical intraepithelial neoplasia and colorectal adenoma. ^25–27. However, the findings are inconclusive. Brown, R. B. et al. illustrated that in middle-aged women living in the United States, higher dietary phosphorus intake appeared to be linked to an elevated risk of breast cancer²⁸. In summary, while phosphorus is crucial for human health, its ideal intake and sources require further investigation. Dietary phosphorus intake may exert varying health effects across different populations and within specific disease contexts. As outlined in the study by McAlpine, J. N. et al., women with a history of PID exhibit a markedly heightened risk of ovarian cancer, suggesting that PID could contribute to the development of ovarian cancer²⁹. Research conducted by Sesti, F. et al. demonstrated that a diet rich in vitamins, macronutrients, and antioxidants has the potential to enhance the immune system and mitigate free radical damage. This dietary pattern may contribute to alleviating chronic pelvic pain, including that associated with PID.³⁰

Some of the aforementioned studies offer evidence regarding the association between dietary phosphorus and specific gynecological diseases, as well as insights into dietary composition and age-related factors associated with PID. Nonetheless, the accurate link between phosphorus intake and PID remains incompletely elucidated. Hence, the goal of this study was to examine the potential relationship between dietary phosphorus intake and PID by analyzing data from the National Health and Nutrition Examination Survey (NHANES). Gaining insight into the impact of dietary phosphorus intake on PID is valuable for the clinical exploration of adjunctive PID treatment and offers a novel direction for PID management.

Study design and population

The National Health and Nutrition Examination Survey (NHANES), conducted by the National Center for Health Statistics (NCHS), is dedicated to assessing the health and nutritional conditions of individuals across the United States on a national scale.³¹ The information we studied came from cross-sectional studies that were conducted between 2015 and 2018 and stored in the NHANES database, and divided into 2 two-year periods (2015–2016, and 2017–2018). The NHANES research program for the years 2015–2018 received official approval from the esteemed National Center for Health Statistics (NCHS). The database is accessible to researchers who meet the eligibility criteria for its use. The data were gathered from 19,225 respondents from the NHANES between 2015 and 2018. Subsequently, data for 9,449 male respondents were removed. Additionally, participants missing PID data (6,300), dietary phosphorus data (165), and other covariate data (682) were excluded, leading to a final dataset comprising information from 2,629 participants. Figure 1 displays the flow chart for the study.

Dietary phosphorus intake

The dietary phosphorus intake of the participants was calculated using the 24-hour dietary recall method. The first dietary recall interview took place face-to-face at a mobile examination center (MEC), with the second interview being conducted via telephone three to 10 days afterwards. Further details regarding this process can be found in the NHANES Mealth Access Program manual.

Examination of PID

The "RHQ078" questionnaire was used to determine the presence of PID by asking whether the individual or their partner had received treatment for an infection in reproductive organs such as the fallopian tubes, uterus, or ovaries, whether the individual or their partner had received treatment for an infection in reproductive organs such as the fallopian tubes, uterus, or ovaries, commonly known as pelvic infection, pelvic inflammatory disease, or PID. Participants who selected "Yes" were grouped under PID, while those who selected "No" were grouped under without-PID. Those who refused to participate, gave a vague answer, or did not complete the PID diagnosis questionnaire were excluded from the study. ³²

Assessment of covariates

Based on prior reports ³³ on dietary phosphorus and pelvic inflammation-related diseases, the following relevant covariates were included in the analysis: age, race, marital status, educational level, poverty-to-income ratio (PIR), body mass index(BMI), hypertension, regular menstruation, diabetes status, and smoking status. We used the following ethnic and racial categories: Mexican American, non-Hispanic Black, non-Hispanic White, other Latinos, and other ethnicities - including multiracial. Marital status was grouped into married/living with a partner, unmarried, and divorced/separated/widowed. Educational attainment was categorized as less than high school, high school, or more than high school. The PIR is segmented into three categories: low, medium, and high. BMI (kg/m2) was divided into three categories: <25, >=25 and < = 30, > 30. We divided the participants into three categories based on their smoking status: never-smokers, former smokers (current nonsmokers), and current smokers. Our approach to diagnosing hypertension included using the criteria of a systolic blood pressure ≥ 140mmHg and/or a diastolic blood pressure ≥ 90mmHg, independent of the effects of antihypertensive drugs. The criteria for diagnosing diabetes included the following: (1) doctor's diagnosis; (2) after an oral glucose tolerance test or random blood glucose level of ≥ 11.1 mmol/L, indicating elevated blood glucose levels; (3) fasting blood glucose of ≥ 7.0mmo1/L; (4) hemoglobin A1C ≥ 6.5%; and (5) use of oral diabetes medication or intramuscular insulin.

Statistical analysis

In our analysis, the means and proportions were examined for significant differences using one-way ANOVA, the Kruskal-Wallis H test, and the chi-square test. We evaluated various models by progressively adjusting for different risk factors. The raw model did not consider any potential confounding variables. Model I, however, adjusted for variances in age and race; in Model II, all covariates were regulated. We divided the study population into three percentiles based on dietary phosphorus intake. The first quantile, Q1, ranges from 8 to 935 mg. The second quantile, Q2, ranges from 935 to 1367 mg. The last quantile, Q3, ranges from 1367 to 5582 mg. The adjusted odds ratio (OR) was derived from these data, with a 95% confidence interval (CI) included. To further explore the relationship between changes in phosphorus intake and the incidence of PID, we utilized multivariate logistic regression analysis and performed smooth curve fitting. Subgroup analyses were conducted to assess the robustness of the primary findings. All statistical analyses were conducted using the R package (R Foundation; http://www.r-project.org; Version 3.4.3) and empower(R) (www.empowerstats.com) by X&Y Solutions, Boston, MA. Statistical significance was determined at a p-value < 0.05.

Participant characteristics

The study participants' characteristics are outlined in Table 1. A total of 2,629 female participants met the eligibility criteria for the study, 165 of whom received a diagnosis of PID. The average age of the participants was 39.8250 ± 11.4785 years. Compared with the non-PID group, the PID group exhibited the following characteristics: older age, a heightened risk of hypertension, irregular menstrual cycles, and a history of current or past smoking (p < 0.05). Education level and diabetes status were not found to be relevant factors. Furthermore, more PID patients were married or cohabiting with a partner, had a better economic status, and had a BMI > 30 kg/m² (p < 0.05).

Table 1

Baseline characteristics
	Overall N = 2629	No PID N = 2464	PID N = 165
Age (years), Mean ± SD	39.8250 ± 11.4785	39.6153 ± 11.4968	42.9576 ± 10.7569
Race, N (%)
Mexican American	453 (17.2309)	434 (17.6136)	19 (11.5152)
Non-Hispanic Black	587 (22.3279)	535 (21.7127)	52 (31.5152)
Non-Hispanic White	868 (33.0164)	813 (32.9951)	55 (33.3333)
Other Hispanic	281 (10.6885)	265 (10.7549)	16 (9.6970)
Other race - including multi-racial	440 (16.7364)	417 (16.9237)	23 (13.9394)
Marital Status, N (%)
Married/Living with partner	1558 (59.2621)	1468 (59.5779)	90 (54.5455)
Never married	606 (23.0506)	578 (23.4578)	28 (16.9697)
Divorced/Separated/Widowed	465 (17.6873)	418 (16.9643)	47 (28.4848)
Educational Level, N (%)
Less than high school	394 (14.9867)	366 (14.8539)	28 (16.9697)
High school	539 (20.5021)	499 (20.2516)	40 (24.2424)
More than high school	1696 (64.5112)	1599 (64.8945)	97 (58.7879)
PIR, N (%)
Low	579 (22.0236)	531 (21.5503)	48 (29.0909)
Medium	1107 (42.1073)	1024 (41.5584)	83 (50.3030)
High	943 (35.8692)	909 (36.8912)	34 (20.6061)
BMI, N (%)
< 25	758 (28.8323)	725 (29.4237)	33 (20.0000)
>=25, <=30	664 (25.2568)	623 (25.2841)	41 (24.8485)
> 30	1207 (45.9110)	1116 (45.2922)	91 (55.1515)
Hypertension, N (%)
No	2357 (89.6539)	2219 (90.0568)	138 (83.6364)
Yes	272 (10.3461)	245 (9.9432)	27 (16.3636)
Regular menstruation, N (%)
No	840 (31.9513)	764 (31.0065)	76 (46.0606)
Yes	1789 (68.0487)	1700 (68.9935)	89 (53.9394)
Diabetes, N (%)
No	2415 (91.8600)	2267 (92.0049)	148 (89.6970)
Yes	214 (8.1400)	197 (7.9951)	17 (10.3030)
Smoke, N (%)
Never	1778 (67.6303)	1709 (69.3588)	69 (41.8182)
Former	378 (14.3781)	336 (13.6364)	42 (25.4545)
Now	473 (17.9916)	419 (17.0049)	54 (32.7273)
Mean ± SD: P value was calculated by one-way ANOVA (normal distribution) and the Kruskal-Wallis H (skewed distribution) test.
% for categorical variables: P value was calculated by the chi-square test.
Abbreviations: PID: pelvic inflammatory disease; PIR: poverty income ratio; BMI: body mass index

Variables influencing PID occurrence

The results of the univariate analysis regarding the incidence of PID (Table 2) revealed significant positive correlations between PID and the following factors: age, non-Hispanic black ethnicity, divorced/separated/widowed marital status, BMI > 30 kg/m², hypertension, and former or current smoking (p < 0.05). Additionally, women with a high PIR or regular menstrual cycles exhibited a decreased risk of PID.

Table 2

**The Univariate Analysis**
Variable	OR_95CI	P-value
Age	1.0262 (1.0118, 1.0408)	0.000328
Race
Mexican American	1(Ref)
Non-Hispanic Black	2.2202 (1.2933, 3.8113)	0.003818
Non-Hispanic White	1.5453 (0.9056, 2.6368)	0.110413
Other Hispanic	1.3791 (0.6971, 2.7286)	0.355780
Other Race - including Multi-Racial	1.2599 (0.6762, 2.3473)	0.466817
Marital Status
Married/Living with partner	1(Ref)
Never married	0.7902 (0.5115, 1.2206)	0.288461
Divorced/Separated/Widowed	1.8340 (1.2680, 2.6528)	0.001278
Educational Level
Less Than High School	1(Ref)
High School	1.0478 (0.6346, 1.7300)	0.855151
More Than High School	0.7930 (0.5130, 1.2257)	0.296488
PIR
Low	1(Ref)
Medium	0.8967 (0.6190, 1.2988)	0.563989
High	0.4138 (0.2633, 0.6504)	0.000131
BMI
< 25	1(Ref)
>=25, <=30	1.4458 (0.9030, 2.3149)	0.124710
> 30	1.7914 (1.1900, 2.6968)	0.005214
Hypertension
No	1(Ref)
Yes	1.7720 (1.1492, 2.7324)	0.009611
Regular menstruation
No	1(Ref)
Yes	0.5263 (0.3830, 0.7232)	0.000075
Diabetes
No	1(Ref)
Yes	1.3218 (0.7838, 2.2292)	0.295382
Smoke
Never	1(Ref)
Former	3.0960 (2.0732, 4.6235)	< 0.000001
Now	3.1921 (2.2009, 4.6296)	< 0.000001

Abbreviations: PID: pelvic inflammatory disease; PIR: poverty income ratio; BMI: body mass index

Associations between phosphorus levels and the incidence of PID

Multifactor logistic regression analysis was carried out to further explore the connection between dietary phosphorus intake and PID, as shown in Table 3. Significant findings regarding the association between dietary phosphorus intake and PID were consistent across both unadjusted and adjusted models (p < 0.05). Based on dietary phosphorus intake, the study population was divided into three percentiles based on dietary phosphorus intake. The critical values for the three quantiles were as follows: Q1 (8 mg ≤ Q1 ≤ 935 mg), Q2 (935 mg < Q2 ≤ 1367 mg), and Q3 (1367 mg < Q3 ≤ 5582 mg). Moreover, in the high-dose subgroup Q3 (1367 ~ 5582 mg), dietary phosphorus was significantly correlated with PID according to both the unadjusted and adjusted models (P < 0.05). In addition, taking into account all potential factors that could affect the outcome, the high-intake phosphorus group (Q3) showed a 38.45% reduction in the OR of PID for an additional milligram of phosphorus (OR = 0.6155, 95% CI = 0.4024 ~ 0.9414, P = 0.025198). Smicker curve fitting was conducted to visualize the results, as shown in Fig. 2. This study further revealed a significant negative linear correlation between dietary phosphorus intake and PID, indicating that a higher intake of phosphorus is linked to a lower likelihood of PID.

Table 3

Relationship between PHOSPHORUS and PID.
	Unadjusted Model OR (95%Cl) P value	Model I OR (95%Cl) P value	Model II OR (95%Cl) P value
phosphorus(mg)	0.9994 (0.9991, 0.9997) 0.000430	0.9995 (0.9992, 0.9998) 0.002655	0.9996 (0.9993, 0.9999) 0.011260
phosphorus(mg)
Q1 (8 -935)	1.0 [Reference]	1.0 [Reference]	1.0 [Reference]
Q2 (935–1367)	0.8436 (0.5880, 1.2102) 0.355538	0.9028 (0.6269, 1.3002) 0.582713	0.9695 (0.6663, 1.4106) 0.871409
Q3 (1367–5582)	0.5139 (0.3408, 0.7750) 0.001494	0.5539 (0.3655, 0.8392) 0.005328	0.6155 (0.4024, 0.9414) 0.025198
P for trend	0.7286 (0.5982, 0.8874) 0.001651	0.7580 (0.6212, 0.9248) 0.006343	0.7990 (0.6516, 0.9797) 0.030960
Unadjusted model did not adjust for any confounding factors
Model I adjusted for Age; Race.
Mode II adjusted for Age; Race; Marital Status; Educational Level; PIR; BMI; Regular Menstruation; Diabetes; Hypertension; Smoke.

Subgroup analyses for the impact of dietary phosphorus on the incidence of PID

Table 4 shows the stratification of age, race, marital status, educational level, PIR, BMI, hypertension status, diabetes status, smoking status, and menstrual cycle. Across all predefined exploratory subgroup analyses, the odds ratio (OR) consistently demonstrated a relatively stable negative correlation (OR < 1) across all subgroups except for the subgroup < 30 years of age. Specifically, a correlation was found in the data indicating that lower phosphorus intake in the diet was linked to a decreased risk of PID among individuals aged 40 to 50 years, non-Hispanic whites, individuals who are married or cohabiting, those with at least a high school education, individuals with a lower PIR, those with a BMI between 25 and 30, individuals without hypertension, and those with irregular menstrual cycles (p < 0.05).

Table 4

Subgroup analyses of the impact of dietary phosphorus on the prevalence of PID
Outcome: Risk of PID
Subgroup	Participants	Q1(8 -935)	Q2 (935–1367)	Q3 (1367–5582)	Tatal
Age(years)
< 30	639	1.0 [Reference]	0.9942 (0.9850, 1.0034) 0.2148	1.0006 (0.9985, 1.0027) 0.6004	1.0003 (0.9995, 1.0011) 0.4568
>=30, < 40	640	1.0 [Reference]	0.9984 (0.9937, 1.0031) 0.5091	0.9984 (0.9961, 1.0008) 0.1914	0.9994 (0.9987, 1.0001) 0.0775
>=40, < 50	670	1.0 [Reference]	1.0000 (0.9950, 1.0049) 0.9844	1.0010 (0.9996, 1.0023) 0.1789	0.9992 (0.9986, 0.9999) 0.0241
>=50	680	1.0 [Reference]	0.9982 (0.9942, 1.0023) 0.3938	0.9974 (0.9941, 1.0008) 0.1403	0.9997 (0.9991, 1.0003) 0.3259
Race
Mexican American	453	1.0 [Reference]	0.9992 (0.9915, 1.0071) 0.8500	0.9999 (0.9978, 1.0021) 0.9604	1.0000 (0.9991, 1.0008) 0.9813
Non-Hispanic Black	587	1.0 [Reference]	1.0014 (0.9965, 1.0062) 0.5837	0.9993 (0.9974, 1.0012) 0.4545	0.9998 (0.9993, 1.0004) 0.5144
Non-Hispanic White	868	1.0 [Reference]	0.9958 (0.9911, 1.0005) 0.0800	1.0000 (0.9980, 1.0021) 0.9643	0.9991 (0.9984, 0.9998) 0.0074
Other Hispanic	281	1.0 [Reference]	0.8862 (0.0000, inf.) 0.9995	0.9954 (0.9868, 1.0041) 0.2995	0.9994 (0.9983, 1.0005) 0.3061
Other Race - including Multi-Racial	440	1.0 [Reference]	0.9958 (0.9860, 1.0057) 0.4058	0.9979 (0.9935, 1.0023) 0.3520	0.9999 (0.9990, 1.0008) 0.7970
Marital Status
Married/Living with partner	1558	1.0 [Reference]	0.9975 (0.9944, 1.0006) 0.1180	1.0004 (0.9994, 1.0014) 0.4573	0.9995 (0.9991, 1.0000) 0.0376
Never married	606	1.0 [Reference]	0.9967 (0.9882, 1.0052) 0.4480	0.9990 (0.9964, 1.0015) 0.4314	0.9999 (0.9992, 1.0006) 0.7891
Divorced/Separated/Widowed	465	1.0 [Reference]	1.0014 (0.9965, 1.0063) 0.5807	0.9973 (0.9932, 1.0014) 0.1962	0.9995 (0.9988, 1.0002) 0.1661
Educational Level
Less than high school	394	1.0 [Reference]	1.0013 (0.9932, 1.0094) 0.7588	0.9993 (0.9965, 1.0021) 0.6027	0.9998 (0.9990, 1.0006) 0.5790
High school	539	1.0 [Reference]	1.0021 (0.9948, 1.0095) 0.5789	1.0001 (0.9983, 1.0019) 0.9506	0.9997 (0.9990, 1.0003) 0.3219
More than high school	1696	1.0 [Reference]	0.9978 (0.9949, 1.0007) 0.1436	0.9997 (0.9985, 1.0008) 0.5677	0.9995 (0.9991, 1.0000) 0.0370
PIR
Low	579	1.0 [Reference]	1.0010 (0.9884, 1.0138) 0.8774	0.9992 (0.9966, 1.0017) 0.5185	0.9992 (0.9986, 0.9999) 0.0220
Medium	1107	1.0 [Reference]	0.9984 (0.9951, 1.0016) 0.3220	0.9994 (0.9982, 1.0006) 0.3032	0.9998 (0.9994, 1.0003) 0.4464
High	943	1.0 [Reference]	0.9959 (0.9911, 1.0007) 0.0939	1.0020 (0.9993, 1.0048) 0.1417	0.9997 (0.9989, 1.0005) 0.4108
BMI(Kg/m2)
< 25	758	1.0 [Reference]	0.9888 (0.9808, 0.9969) 0.0066	0.9994 (0.9971, 1.0017) 0.6005	0.9999 (0.9992, 1.0005) 0.6972
>=25, <=30	664	1.0 [Reference]	0.9981 (0.9938, 1.0025) 0.3938	0.7388 (0.0000, inf.) 0.9943	0.9990 (0.9982, 0.9998) 0.0145
> 30	1207	1.0 [Reference]	1.0003 (0.9968, 1.0039) 0.8606	0.9999 (0.9990, 1.0008) 0.8360	0.9997 (0.9993, 1.0001) 0.1333
Hypertension
No	2357	1.0 [Reference]	0.9982 (0.9956, 1.0007) 0.1650	1.0000 (0.9992, 1.0008) 0.9686	0.9996 (0.9993, 1.0000) 0.0320
Yes	272	1.0 [Reference]	1.0011 (0.9926, 1.0098) 0.7956	0.8804 (0.0000, inf.) 0.9995	0.9993 (0.9983, 1.0002) 0.1368
Regular menstruation
No	840	1.0 [Reference]	0.9991 (0.9955, 1.0027) 0.6194	0.9993 (0.9974, 1.0011) 0.4493	0.9994 (0.9989, 1.0000) 0.0339
Yes	1789	1.0 [Reference]	0.9976 (0.9944, 1.0009) 0.1495	0.9997 (0.9986, 1.0007) 0.5392	0.9996 (0.9992, 1.0001) 0.0937
Diabetes
No	2415	1.0 [Reference]	0.9988 (0.9963, 1.0013) 0.3364	0.9999 (0.9991, 1.0008) 0.8917	0.9996 (0.9993, 1.0000) 0.0432
Yes	214	1.0 [Reference]	0.9993 (0.9894, 1.0093) 0.8894	0.9834 (0.0000, inf.) 1.0000	0.9977 (0.9959, 0.9996) 0.0148
Smoke
Never	1778	1.0 [Reference]	0.9995 (0.9961, 1.0028) 0.7562	0.9993 (0.9979, 1.0007) 0.3258	0.9997 (0.9992, 1.0002) 0.1883
Former	378	1.0 [Reference]	0.9961 (0.9903, 1.0018) 0.1806	1.0019 (0.9993, 1.0044) 0.1508	0.9994 (0.9986, 1.0001) 0.1053
Now	473	1.0 [Reference]	0.9997 (0.9939, 1.0055) 0.9239	1.0000 (0.9987, 1.0012) 0.9583	0.9996 (0.9990, 1.0001) 0.1453
The multivariate logistic model adjusted for age; race; marital status; educational level; PIR; BMI; regular menstruation; diabetes; hypertension; and smoke, except for the variable that was stratified.
Explanation for inf.: The model failed because of the small sample size.

Moreover, the association between dietary phosphorus intake and PID remained significant and linearly negative among individuals aged 40 to 50 years, non-Hispanic whites, married or cohabiting individuals, those with a high school education or higher, individuals with a lower PIR, those with a BMI between 25 and 30, individuals without hypertension, and those with irregular menstrual cycles (Fig. 3, 4, 5, 6, 7, 8, 10). The evidence points toward a connection between higher dietary phosphorus intake and a reduced risk of PID. Furthermore, regardless of diabetes status, a lower risk of developing PID was significantly linked to reduced dietary phosphorus intake (p < 0.05). This conclusion was consistent when smooth curve fitting techniques were used (Fig. 11). Similarly, regardless of smoking status, dietary phosphorus intake was negatively associated with the risk of developing PID, although the results were not significant (p > 0.05).

The goal of this cross-sectional study was to investigate how dietary phosphorus intake is related to PID in females. Our study revealed a strong correlation between increased dietary phosphorus intake and a decreased likelihood of developing PID. Despite from past studies that have mainly examined how dietary phosphorus impacts bone health, frequently highlighting the possible adverse consequences of consuming too much on bone strength, our study highlights the substantial implications of phosphorus intake for PID risk. This underscores the importance of adopting a broader dietary perspective that recognizes the role of phosphorus not only in bone health but also in lowering susceptibility to PID.^{34, 35 36 14} Recent studies suggest that consuming phosphorus-rich foods may help protect against cervical intraepithelial neoplasia (CIN) and colorectal adenomas. Interestingly, these findings suggest a potential relationship between dietary phosphorus and PID. ^25–27 Although dietary phosphorus has been associated with inflammation prevention, the precise mechanisms underlying this relationship remain unclear. ³⁷ Furthermore, research conducted on mice has revealed the link between dietary phosphorus intake and inflammation. The study indicated that an extended high-phosphate diet had a significant detrimental impact on bone density and led to chronic low-grade inflammation.³⁸ Low phosphorus levels have been associated with increased hepatic lipid deposition, oxidative stress, and inflammatory responses. Conversely, high phosphorus levels may exert inhibitory effects on inflammation to some extent ³⁹. These findings suggest that a decrease in dietary phosphorus intake is associated with a decreased likelihood of developing PID.

Although the precise mechanism through which dietary phosphorus mitigates the risk of PID remains unclear, various potential biological pathways exist. PID is an inflammatory disease, and dietary phosphorus may play a role by affecting inflammatory pathways. Studies have demonstrated the ability of phosphorus to reduce IL-1β levels⁴⁰, with IL-1β, IL-6, IL-8, and TNF-α implicated in PID pathogenesis⁴¹. Thus, phosphorus may mitigate PID risk through this pathway. Phosphorus plays a critical role in maintaining the well-being of all life forms, owing to its pivotal role in the structure and function of numerous critical biological molecules.^{42 43} Notably, phosphorus plays a crucial role in cellular energy metabolism because it constitutes a fundamental component of ATP, the primary energy molecule. ⁴⁴ In addition to its function in intracellular energy transfer, the nucleotide ATP also plays a critical role in extracellular signaling reactions involved in inflammation and immune responses. First, immune cells require an adequate supply of ATP to ensure the effective performance of immune functions, including phagocytosis of pathogens and generation of immune responses. Neisseria gonorrhea and Chlamydia trachomatis are two of the most common pathogens associated with PID. Enhancing the function of macrophages and their bactericidal activities may accelerate the clearance of these pathogens, thereby reducing the risk of PID. ⁴⁵ Thus, increased dietary phosphorus intake contributes to maintaining immune system vitality, potentially lowering the risk of PID, particularly that induced by pathogens. Furthermore, in the synthesis of hormones, ATP serves as the central mediator of energy transfer. This is especially evident in the biosynthesis of sex hormones, such as estrogen and progesterone, which rely on intracellular energy levels primarily derived from ATP breakdown⁴⁶. Estrogenic activity can influence different pathways in the body, such as immune responses^47–49. Specifically, E2 regulates the immune system's proinflammatory signals and pathways^{50, 51 52}. Thus, dietary phosphorus can influence PID through energy metabolism and immune response pathways.

The varying levels of calcium and phosphorus intake may affect the susceptibility of these groups to certain diseases, including PID. These findings suggest that nutritional interventions for phosphorus may need to be personalized based on age and race, especially for adults older than 50 years, who may require increased attention to maintain adequate phosphorus intake. This targeted approach could help mitigate the increased risk of inflammation-related diseases associated with age-related changes in nutrient absorption and dietary habits.

Nevertheless, this study has several limitations. First, the lack of causality can be attributed to the cross-sectional nature of the study. The diet frequently involves complex additive effects and biological interactions due to the combination of multiple nutrients and nonnutrients⁵³. Even after accounting for established covariates, there may still be minor unknown or uncontrolled factors, such as sexual activity, history of sexually transmitted infections, and recent pelvic surgery^{54, 55}, which may influence the results. Additionally, limitations in sample selection and data collection may restrict the generalizability of the results. Despite efforts to incorporate relevant confounding factors, not all confounding factors could be addressed. Last, the NHANES data are subject to inherent sampling errors that must be taken into consideration. Hence, these results necessitate validation in future studies employing more rigorous experimental designs.

Phosphorus intake was shown to be inversely related to the incidence of PID in our study. Nevertheless, a precise dose-response relationship requires further epidemiological investigation. Additionally, both excessively high and low phosphorus levels can be detrimental to human health. The implications of excessive phosphorus intake, which is associated with various health issues such as osteoporosis and cardiovascular diseases, underscore the importance of prudent management of dietary phosphorus levels⁵⁶ . Future research should concentrate on gathering more diverse and extensive data, encompassing variations in lifestyle, dietary habits, and additional elements, to substantiate the specific relationship between phosphorus intake and PID risk, and to determine the optimal phosphorus intake level for health.

Ethics statement

In line with the Declaration of Helsinki, the Ethics Committee of the National Centre for Health Statistics approved for this study. The study did not involve the personal information or privacy of the participants, and they were not exposed to any potential harm. Before participating in the study, all participants provided written informed consent. The electronic download process facilitated the efficient retrieval of all relevant information, which was conveniently accessible at a designated location at https://wwwn.cdc.gov/nchs/nhanes/default.aspx.

Permission to publish

Does not apply.

Data availability status

The NHANES repository, located at https://www.cdc.gov/nchs/nhanes/, allows for the exploration of the datasets employed in this research.

Rivaling agendas

The authors have confirmed the absence of situations involving conflicting interests.

Funding

Funding was not allocated for this study.

Authors' contributions

The contributions of MHM, ZYF, and CZR included the collection, evaluation, formulation, and drafting of the data for academic writing. ZYP, PJ, CY, LHB, and LJW aided in the development of the manuscript. Additionally, the MHM played a pivotal role in conceptualizing and managing the project. The manuscript has been approved by all the authors.

Acknowledgments

The authors extend their gratitude to the participants who generously gave their time and effort while gathering data for the NHANES project.

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No competing interests reported.

WITHDRAWN: A Cross-sectional Study on Pelvic Inflammatory Disease Prevalence and Dietary Phosphorus using NHANES Data from 2015-2018

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Editorial Note

Abstract

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Background

Methods

Statistical analysis

Results

Discussion

Conclusion

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References

Additional Declarations

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