The Association between Maternal Oral Inflammation and Neutrophil Phenotypes and Poly-Unsaturated Fatty Acids Composition in Human Milk: A Prospective Cohort Study
Abstract
:1. Introduction
2. Materials and Methods
2.1. Study Population and Patient Selection
2.2. Maternal Demographic Characteristics and Dietary Intake
2.3. Oral Rinse Samples Collection and Processing
2.4. Human Milk Samples Collection and Processing
2.5. Flow Cytometry
2.6. Cell Sorting, Cytospin Preparation and Staining
2.7. Fatty Acids Analysis in Human Milk
2.8. Statistical Analysis and Sample Size Estimate
3. Results
3.1. Participants’ Descriptive Characteristics
3.2. Participants’ Oral Inflammatory Load
3.3. Maternal Dietary Intake
3.4. hmPMNs Had Lower Activation State Compared to oPMNs
3.5. Mothers with Moderate to Severe OIL Had hmPMNs with Higher Expression Levels of CD14 Biomarker and Lower Expression Levels of CD64 Biomarker during Lactation, Compared to Mothers with Healthy OIL
3.6. Mothers with Moderate and Severe OIL Had Higher Levels of n-6 PUFA; Docosapentaenoic Acid (DPA) in Their Human Milk at Baseline, Compared to Mothers with Healthy OIL
3.7. Mothers with Moderate to Severe OIL Had Lower Levels of C20:5n-3 (EPA) LCPUFA during Lactation, Compared to Mothers with Healthy OIL
3.8. CD64 Surface Expression on hmPMNs Was Higher in Mothers Whose Infants Had a Health Condition Compared to the Mothers of Healthy Infants
3.9. Higher Levels of Arachidonic Acid and C22:5n-6 FA Were Observed in the Human Milk of the Mothers Whose Infants Had a Health Condition Compared to Healthy Infants
3.10. Correlation between Human Milk PMNs and Their Levels of Activation and the FAs in Human Milk
4. Discussion
Study Limitations and Strengths
5. Conclusions
Supplementary Materials
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Acknowledgments
Conflicts of Interest
References
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Characteristics | Variables | Total N (%) |
---|---|---|
Demographic characteristics | Age (years) | |
(Mean ± SD) | 34.5 ± 4.4 | |
Marital status | ||
Married | 40 (85.1) | |
Single/Unmarried partners | 7 (14.9) | |
Employment status | ||
Employed full-time | 32 (68.1) | |
Employed part-time/Student/unemployed | 15 (31.9) | |
Highest education level | ||
Secondary graduate/Degree/Diploma | 23 (48.9) | |
Post-graduate studies | 24 (51.1) | |
Maternal and infant characteristics | Gestational age at delivery (weeks) | 39.1 ± 1.2 |
(Mean ± SD) | ||
BMI after delivery (kg/m2) | 25.1 ± 3.7 | |
(Mean ± SD) | ||
Infant feeding patterns | ||
Exclusive BF | 32 (64.0) | |
Predominant BF | 11 (22.0) | |
Mixed feeding * | 4 (8.0) | |
Infant sex | ||
Boy | 26 (52.0) | |
Girl | 22 (44.0) | |
Infant health status | ||
Healthy | 39 (78.0) | |
Diseased/Infected | 8 (16.0) | |
Lifestyle and dental history | Brushing at least twice a day | 32 (68.1) |
Flossing at least once per day | 12 (25.1) | |
Dental visit frequency | ||
≥1 visit a year | 38 (80.9) | |
<1 visit a year | 5 (10.6) | |
Only for emergency | 4 (8.5) |
oPMN Counts (×106/10 mL Rinse) | N | Mean ± SD | Median | Minimum | Maximum |
---|---|---|---|---|---|
Total oPMN counts | |||||
Baseline | 50 | 1.38 ± 1.63 | 0.65 | 0 | 6.97 |
Follow-up | 46 | 1.93 ± 4.24 | 0.72 | 0 | 23.56 |
Baseline | |||||
Healthy | 21 | 0.25 ± 0.15 | 0.35 | 0 | 0.47 |
Moderate | 8 | 0.76 ± 0.14 | 0.65 | 0.52 | 0.98 |
Severe | 21 | 2.66 ± 1.89 | 1.89 | 1.01 | 6.97 |
Follow-up | |||||
Healthy | 16 | 0.22 ± 0.15 | 0.29 | 0 | 0.49 |
Moderate | 13 | 0.78 ± 0.13 | 0.7 | 0.5 | 0.93 |
Severe | 17 | 4.59 ± 6.38 | 1.43 | 1.1 | 23.57 |
Neutrophils and CD Biomarkers † | Diseased OIL (n = 20) | |||
---|---|---|---|---|
Estimate β b (95% CI) | p-Value | Adjusted Estimate β c (95% CI) | Adjusted p-Value | |
Absolute hmPMN counts (×106/10 mL) | 0.23 (−0.10, 0.57) | 0.168 | 0.27 (−0.11, 0.65) | 0.17 |
CD16 | −175.72 (−419.60, 68.15) | 0.156 | −172.41 (−447.57, 102.75) | 0.216 |
CD66a | −86.62 (−236.12, 62.88) | 0.253 | −76.77 (−270.10, 116.55) | 0.431 |
CD11b | −6.26 (−175.29, 162.76) | 0.941 | 17.21 (−171.75, 206.17) | 0.856 |
CD18 | 445.38 (−991.48, 1882.25) | 0.539 | 503.41 (−1000.33, 2007.16) | 0.507 |
CD14 | 128.22 (−2.34, 258.80) | 0.054 | 151.25 (14.13, 288.36) | 0.031 |
CD64 | −75.04 (−149.00, −1.07) | 0.047 | −95.35 (−187.69, −3.01) | 0.043 |
CD63 | −26.44 (−145.40, 92.51) | 0.66 | −4.58 (−133.71, 124.54) | 0.944 |
Fatty Acids in Human Milk | Diseased OIL (n = 20) | |||
---|---|---|---|---|
Estimate β b (95% CI) | p-Value | Adjusted Estimate β c (95% CI) | Adjusted p-Value | |
C10:0 | −0.17 (−0.49, 0.14) | 0.269 | −0.15 (−0.50, 0.18) | 0.368 |
C12:0 | −0.80 (−2.06, 0.46) | 0.210 | −0.91 (−2.27, 0.44) | 0.182 |
C14:0 | −0.57 (−1.85, 0.71) | 0.376 | −0.50 (−1.80, 0.79) | 0.440 |
C16:0 | 0.94 (−1.77, 3.65) | 0.492 | 1.63 (−1.29, 4.57) | 0.269 |
C18:0 | 1.27 (0.10, 2.43) | 0.032 | 1.11 (−0.15, 2.39) | 0.084 |
C20:0 | 0.01 (−0.02, 0.06) | 0.439 | 0.01 (−0.04, 0.06) | 0.739 |
C22:0 | 0.01 (−0.04, 0.05) | 0.865 | −0.01 (−0.06, 0.04) | 0.674 |
C23:0 | −0.03 (−0.29, 0.22) | 0.772 | −0.05 (−0.34, 0.24) | 0.719 |
C24:0 | 0.01 (−0.03, 0.04) | 0.731 | 0.01 (−0.03, 0.04) | 0.799 |
SFAs | 0.60 (−4.02, 5.22) | 0.796 | 0.80 (−4.32, 5.93) | 0.756 |
C14:1 | −0.05 (−0.12, 0.02) | 0.192 | −0.01 (−0.09, 0.07) | 0.795 |
C18:1n-7 | −2.97 (−10.66, 4.72) | 0.445 | −1.83 (−10.75, 7.08) | 0.683 |
C18:1n-9 | 4.21 (−4.43, 12.87) | 0.335 | 2.98 (−6.76, 12.74) | 0.543 |
C20:1n-9 | 0.05 (−0.03, 0.13) | 0.240 | 0.03 (−0.05, 0.12) | 0.469 |
C22:1n-9 | −0.07 (−0.21, 0.05) | 0.242 | −0.11 (−0.26, 0.04) | 0.151 |
MUFAs | 1.43 (−3.17, 6.03) | 0.539 | 1.18 (−3.64, 6.01) | 0.627 |
C18:2n-6 (LA) | −1.22 (−6.74, 4.29) | 0.661 | −0.64 (−6.69, 5.39) | 0.831 |
C18:3n-6 (GLA) | 0.00 (−0.04, 0.04) | 0.969 | 0.01 (−0.03, 0.04) | 0.851 |
C20:2n-6 | 0.08 (−0.23, 0.39) | 0.604 | 0.06 (−0.28, 0.42) | 0.705 |
C20:3n-6 | 0.05 (−0.03, 0.15) | 0.233 | 0.03 (−0.07, 0.14) | 0.501 |
C20:4n-6 (AA) | 0.02 (−0.09, 0.14) | 0.687 | −0.01 (−0.13, 0.12) | 0.914 |
C22:2n-6 | 0.71 (−1.18, 2.61) | 0.458 | 0.59 (−1.60, 2.80) | 0.589 |
C22:4n-6 | −0.08 (−0.21, 0.04) | 0.188 | −0.12 (−0.26, 0.01) | 0.088 |
C22:5n-6 | −0.05 (−0.12, 0.01) | 0.075 | −0.04 (−0.11, 0.02) | 0.166 |
N-6 | −1.10 (−7.38, 5.18) | 0.729 | −0.50 (−7.39, 6.38) | 0.884 |
C18:3n-3 (ALA) | 0.21 (−0.50, 0.93) | 0.558 | −0.06 (−0.85, 0.73) | 0.880 |
C20:5n-3 (EPA) | −0.11 (−0.22, −0.01) | 0.029 | −0.12 (−0.24, 0.00) | 0.056 |
C22:5n-3 | −0.06 (−0.19, 0.06) | 0.336 | −0.11 (−0.25, 0.03) | 0.132 |
C22:6n-3 (DHA) | −0.04 (−0.23, 0.14) | 0.647 | −0.06 (−0.27, 0.14) | 0.536 |
N-3 | −0.10 (−0.96, 0.75) | 0.807 | −0.42 (−1.36, 0.51) | 0.369 |
PUFAs | −0.84 (−7.41, 5.72) | 0.799 | −0.48 (−7.62, 6.66) | 0.894 |
N6/N3 | 4.33 (−7.19, 15.86) | 0.457 | 5.52 (−7.54, 18.59) | 0.402 |
Neutrophils and CD Markers | Infants with a Health Condition (n = 14) c | |||
---|---|---|---|---|
Estimate β a (95% CI) | p-Value | Adjusted Estimate β b (95% CI) | Adjusted p-Value | |
Absolute hmPMN counts (×106/10 mL) | −0.13 (−0.49, 0.21) | 0.288 | −0.05 (−0.30, 0.18) | 0.624 |
CD16 | −46.23 (−306.54, 214.07) | 0.553 | 60.94 (−170.74, 292.63) | 0.599 |
CD66a | −33.50 (−189.92, 122.91) | 0.890 | −36.03 (−155.85, 83.78) | 0.547 |
CD11b | 10.91 (−169.38, 191.21) | 0.602 | −26.22 (−142.45, 90.00) | 0.650 |
CD18 | 861.03 (−635.55, 2357.63) | 0.423 | 359.51 (−781.69, 1500.73) | 0.529 |
CD14 | 81.35 (−51.31, 214.02) | 0.392 | 38.05 (−37.85, 113.95) | 0.316 |
CD64 | 100.25 (27.69, 172.80) | 0.019 | 85.65 (21.97, 149.32) | 0.009 |
CD63 | −4.75 (−121.62, 112.11) | 0.183 | −54.96 (−150.39, 40.47) | 0.250 |
Fatty Acids in Human Milk | Infants with a Health Condition (n = 14) | |||
---|---|---|---|---|
Estimate β a (95% CI) | p-Value | Adjusted Estimate β b (95% CI) | Adjusted p-Value | |
C10:0 | −0.14 (−0.49, 0.20) | 0.257 | −0.16 (−0.43, 0.11) | 0.241 |
C12:0 | −0.79 (−2.21, 0.63) | 0.219 | −0.63 (−1.76, 0.49) | 0.267 |
C14:0 | −0.99 (−2.42, 0.43) | 0.121 | −0.45 (−1.51, 0.61) | 0.399 |
C16:0 | −2.61 (−5.58, 0.35) | 0.057 | −1.51 (−3.85, 0.82) | 0.200 |
C18:0 | −0.17 (−1.49, 1.14) | 0.415 | −0.92 (−1.95, 0.11) | 0.081 |
C20:0 | −0.02 (−0.07, 0.02) | 0.564 | −0.02 (−0.06, 0.01) | 0.193 |
C22:0 | 0.03 (−0.01, 0.08) | 0.055 | 0.02 (−0.01, 0.06) | 0.152 |
C23:0 | 0.00 (−0.26, 0.26) | 0.492 | −0.01 (−0.22, 0.19) | 0.902 |
C24:0 | 0.01 (−0.01, 0.03) | 0.003 | 0.03 (0.01, 0.06) | 0.004 |
SFAs | −4.42 (−9.34, 0.49) | 0.028 | −3.34 (−7.39, 0.69) | 0.103 |
C14:1 | −0.01 (−0.09, 0.07) | 0.216 | −0.01 (−0.07, 0.04) | 0.646 |
C18:1n-7 | −2.52 (−10.96, 5.91) | 0.326 | −2.17 (−7.53, 3.17) | 0.417 |
C18:1n-9 | 0.29 (−9.19, 9.79) | 0.575 | −0.11 (−6.60, 6.37) | 0.971 |
C20:1n-9 | −0.04 (−0.14, 0.05) | 0.845 | −0.01 (−0.08, 0.07) | 0.898 |
C22:1n-9 | −0.01 (−0.16, 0.12) | 0.512 | 0.08 (−0.04, 0.20) | 0.182 |
MUFAs | −2.14 (−7.01, 2.71) | 0.540 | −2.39 (−5.76, 0.97) | 0.160 |
C18:2n-6 (LA) | 3.01 (−2.58, 8.62) | 0.140 | 2.86 (−1.10, 6.83) | 0.153 |
C18:3n-6 (GLA) | −0.01 (−0.05, 0.03) | 0.762 | −0.01 (−0.04, 0.02) | 0.664 |
C20:2n-6 | 0.21 (−0.11, 0.54) | 0.138 | 0.19 (−0.09, 0.47) | 0.180 |
C20:3n-6 | −0.01 (−0.12, 0.08) | 0.773 | 0.01 (−0.07, 0.10) | 0.719 |
C20:4n-6 (AA) | 0.09 (−0.03, 0.22) | 0.009 | 0.12 (0.02, 0.21) | 0.013 |
C22:2n-6 | 0.09 (−1.96, 2.15) | 0.683 | −0.14 (−1.96, 1.66) | 0.873 |
C22:4n-6 | 0.04 (−0.07, 0.16) | 0.041 | 0.08 (−0.01, 0.16) | 0.065 |
C22:5n-6 | 0.09 (0.02, 0.16) | 0.010 | 0.06 (0.01, 0.12) | 0.015 |
N-6 | 4.60 (−1.78, 10.99) | 0.155 | 3.73 (−0.83, 8.30) | 0.107 |
C18:3n-3 (ALA) | 0.78 (0.05, 1.52) | 0.036 | 0.44 (−0.17, 1.07) | 0.155 |
C20:5n-3 (EPA) | −0.04 (−0.15, 0.06) | 0.902 | −0.04 (−0.12, 0.04) | 0.319 |
C22:5n-3 | −0.01 (−0.14, 0.11) | 0.155 | 0.06 (−0.04, 0.16) | 0.264 |
C22:6n-3 (DHA) | 0.11 (−0.09, 0.31) | 0.06 | 0.11 (−0.04, 0.27) | 0.171 |
N-3 | 0.83 (−0.03, 1.70) | 0.014 | 0.67 (−0.02, 1.37) | 0.059 |
PUFAs | 5.21 (−1.28, 11.71) | 0.060 | 4.27 (−0.46, 9.01) | 0.076 |
N6/N3 | −5.51 (−18.27, 7.24) | 0.321 | −4.07 (−13.48, 5.33) | 0.388 |
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Badewy, R.; Azarpazhooh, A.; Tenenbaum, H.; Connor, K.L.; Lai, J.Y.; Sgro, M.; Bazinet, R.P.; Fine, N.; Watson, E.; Sun, C.; et al. The Association between Maternal Oral Inflammation and Neutrophil Phenotypes and Poly-Unsaturated Fatty Acids Composition in Human Milk: A Prospective Cohort Study. Cells 2022, 11, 4110. https://doi.org/10.3390/cells11244110
Badewy R, Azarpazhooh A, Tenenbaum H, Connor KL, Lai JY, Sgro M, Bazinet RP, Fine N, Watson E, Sun C, et al. The Association between Maternal Oral Inflammation and Neutrophil Phenotypes and Poly-Unsaturated Fatty Acids Composition in Human Milk: A Prospective Cohort Study. Cells. 2022; 11(24):4110. https://doi.org/10.3390/cells11244110
Chicago/Turabian StyleBadewy, Rana, Amir Azarpazhooh, Howard Tenenbaum, Kristin L. Connor, Jim Yuan Lai, Michael Sgro, Richard P. Bazinet, Noah Fine, Erin Watson, Chunxiang Sun, and et al. 2022. "The Association between Maternal Oral Inflammation and Neutrophil Phenotypes and Poly-Unsaturated Fatty Acids Composition in Human Milk: A Prospective Cohort Study" Cells 11, no. 24: 4110. https://doi.org/10.3390/cells11244110
APA StyleBadewy, R., Azarpazhooh, A., Tenenbaum, H., Connor, K. L., Lai, J. Y., Sgro, M., Bazinet, R. P., Fine, N., Watson, E., Sun, C., Saha, S., & Glogauer, M. (2022). The Association between Maternal Oral Inflammation and Neutrophil Phenotypes and Poly-Unsaturated Fatty Acids Composition in Human Milk: A Prospective Cohort Study. Cells, 11(24), 4110. https://doi.org/10.3390/cells11244110