Intake of citrus fruits and vegetables and the intensity of defecation urgency syndrome among gynecological cancer survivors

Maria Hedelin, Viktor Skokic, Ulrica Wilderäng, Rebecca Ahlin, Cecilia Bull, Fei Sjöberg, Gail Dunberger, Karin Bergmark, Andrea Stringer, Gunnar Steineck, Maria Hedelin, Viktor Skokic, Ulrica Wilderäng, Rebecca Ahlin, Cecilia Bull, Fei Sjöberg, Gail Dunberger, Karin Bergmark, Andrea Stringer, Gunnar Steineck

Abstract

Background: Despite the experimental evidence that certain dietary compounds lower the risk of radiation-induced damage to the intestine, clinical data are missing and dietary advice to irradiated patients is not evidence-based.

Materials and methods: We have previously identified 28 intestinal health-related symptoms among 623 gynaecological-cancer survivors (three to fifteen years after radiotherapy) and 344 matched population-based controls. The 28 symptoms were grouped into five radiation-induced survivorship syndromes: defecation-urgency syndrome, fecal-leakage syndrome, excessive mucus discharge, excessive gas discharge and blood discharge. The grouping was based on factor scores produced by Exploratory Factor Analysis in combination with the Variable Cutoff Method. Frequency of food intake was measured by a questionnaire. We evaluated the relationship between dietary intake and the intensity of the five syndromes.

Results: With the exception of excessive mucus discharge, the intensity of all syndromes declined with increasing intake of citrus fruits. The intensity of defecation-urgency and fecal-leakage syndrome declined with combined intake of vegetables and citrus fruits. The intensity of excessive mucus discharge was increased with increasing intake of gluten.

Conclusion: In this observational study, we found an association between a high intake of citrus fruits and vegetables and a lower intensity of the studied radiation-induced cancer survivorship syndromes. Our data suggest it may be worthwhile to continue to search for a role of the diet before, during and after radiotherapy to help the cancer survivor restore her or his intestinal health after irradiation.

Conflict of interest statement

Gunnar Steineck is PI for a study of probiotics sponsored by Probi AB. This does not alter our adherence to PLOS ONE policies on sharing data and materials. There exist no other competing interests.

Figures

Fig 1. Relationships between radiation-induced survivorship syndromes…
Fig 1. Relationships between radiation-induced survivorship syndromes and frequency of citrus intake.
The figure depicts the relationships between frequency of citrus intake (x-axis) and intensities (factor scores) of the five radiation induced syndromes (y-axis: defecation-urgency syndrome, fecal-leakage syndrome, excessive gas discharge, excessive mucus discharge and blood discharge) among long-term gynecological cancer survivors and population controls. Red squares and green triangles denote the mean syndrome intensities within certain citrus intake frequency levels. Vertical black lines stretch between plus-minus the standard error of the mean. Asterisks correspond to significance levels of the Spearman correlations between syndrome intensities and frequency of citrus intake according to: p ≤ 0.001 - ***, 0.001

Fig 2. Relationship between radiation-induced survivorship syndromes…

Fig 2. Relationship between radiation-induced survivorship syndromes and frequency of vegetable and citrus fruit intake.

Fig 2. Relationship between radiation-induced survivorship syndromes and frequency of vegetable and citrus fruit intake.
The figure depicts the relationships between frequency of combined intake of beans and lentils, cabbage and broccoli, onion and garlic, grated vegetables together with citrus fruits (x-axis) and intensities (factor scores) of the two radiation-induced survivorship syndromes (y-axis) defecation-urgency syndrome and fecal-leakage syndrome among long-term gynecological cancer survivors and population controls. Red squares and green triangles denote the mean syndrome intensities within certain vegetable and citrus intake frequency levels. Vertical black lines stretch between plus-minus the standard error of the mean. Asterisks correspond to significance levels of the Spearman correlations between syndrome intensities and frequency of vegetable and citrus intake according to: p ≤ 0.001 - ***, 0.001

Fig 3. Relationship between intensity of excessive…

Fig 3. Relationship between intensity of excessive mucus discharge and frequency of gluten intake.

The…

Fig 3. Relationship between intensity of excessive mucus discharge and frequency of gluten intake.
The figure depicts the relationship between frequency of gluten intake (x-axis) and the intensity (factor scores) of the radiation induced syndrome (y-axis) excessive mucus discharge among long-term gynecological cancer survivors and population controls. Red squares/green triangles denote the mean syndrome intensity within certain gluten intake frequency levels. Vertical black lines stretch between plus-minus the standard error of the mean. Asterisks correspond to significance levels of the Spearman correlations between syndrome intensity and frequency of gluten intake according to: p ≤ 0.001 - ***, 0.001

Fig 4. Relationship between radiation-induced defecation-urgency syndrome…

Fig 4. Relationship between radiation-induced defecation-urgency syndrome and frequency of citrus fruit intake, stratified by…

Fig 4. Relationship between radiation-induced defecation-urgency syndrome and frequency of citrus fruit intake, stratified by those who have changed and those who have not changed dietary behavior after radiotherapy.
The figure depicts the relationship between frequency of citrus fruit intake (x-axis) and the intensity (factor scores) the defecation-urgency syndrome (y-axis) among long-term gynecological cancer survivors stratified according to having or not having made dietary changes after receiving radiotherapy (see the Methods section for detailed information). Red squares and green triangles denote the mean intensities of the syndromes within certain citrus intake frequency levels. Vertical black lines stretch between plus-minus the standard error of the mean. Asterisks correspond to significance levels of the Spearman correlations between syndrome intensity and frequency of citrus intake according to: p ≤ 0.001 - ***, 0.001
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References
    1. Khalid U, McGough C, Hackett C, Blake P, Harrington KJ, Khoo VS, et al. A modified inflammatory bowel disease questionnaire and the Vaizey Incontinence questionnaire are more sensitive measures of acute gastrointestinal toxicity during pelvic radiotherapy than RTOG grading. International journal of radiation oncology, biology, physics. 2006;64(5):1432–41. 10.1016/j.ijrobp.2005.10.007 - DOI - PubMed
    1. Resbeut M, Marteau P, Cowen D, Richaud P, Bourdin S, Dubois JB, et al. A randomized double blind placebo controlled multicenter study of mesalazine for the prevention of acute radiation enteritis. Radiotherapy and oncology: journal of the European Society for Therapeutic Radiology and Oncology. 1997;44(1):59–63. - PubMed
    1. Steineck G, Skokic V, Sjoberg F, Bull C, Alevronta E, Dunberger G, et al. Identifying radiation-induced survivorship syndromes affecting bowel health in a cohort of gynecological cancer survivors. PLoS One. 2017;12(2):e0171461 10.1371/journal.pone.0171461 - DOI - PMC - PubMed
    1. Kuku S, Fragkos C, McCormack M, Forbes A. Radiation-induced bowel injury: the impact of radiotherapy on survivorship after treatment for gynaecological cancers. Br J Cancer. 2013;109(6):1504–12. 10.1038/bjc.2013.491 - DOI - PMC - PubMed
    1. Ferreira MR, Muls A, Dearnaley DP, Andreyev HJ. Microbiota and radiation-induced bowel toxicity: lessons from inflammatory bowel disease for the radiation oncologist. Lancet Oncol. 2014;15(3):e139–47. 10.1016/S1470-2045(13)70504-7 - DOI - PubMed
Show all 56 references
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Grant support
This work was supported by the Swedish Cancer Society to GS, the King Gustav V Jubilee Clinic Cancer Foundation in Göteborg, Sweden to GS and the Swedish state under the ALF agreement in Göteborg. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
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Fig 2. Relationship between radiation-induced survivorship syndromes…
Fig 2. Relationship between radiation-induced survivorship syndromes and frequency of vegetable and citrus fruit intake.
The figure depicts the relationships between frequency of combined intake of beans and lentils, cabbage and broccoli, onion and garlic, grated vegetables together with citrus fruits (x-axis) and intensities (factor scores) of the two radiation-induced survivorship syndromes (y-axis) defecation-urgency syndrome and fecal-leakage syndrome among long-term gynecological cancer survivors and population controls. Red squares and green triangles denote the mean syndrome intensities within certain vegetable and citrus intake frequency levels. Vertical black lines stretch between plus-minus the standard error of the mean. Asterisks correspond to significance levels of the Spearman correlations between syndrome intensities and frequency of vegetable and citrus intake according to: p ≤ 0.001 - ***, 0.001

Fig 3. Relationship between intensity of excessive…

Fig 3. Relationship between intensity of excessive mucus discharge and frequency of gluten intake.

The…

Fig 3. Relationship between intensity of excessive mucus discharge and frequency of gluten intake.
The figure depicts the relationship between frequency of gluten intake (x-axis) and the intensity (factor scores) of the radiation induced syndrome (y-axis) excessive mucus discharge among long-term gynecological cancer survivors and population controls. Red squares/green triangles denote the mean syndrome intensity within certain gluten intake frequency levels. Vertical black lines stretch between plus-minus the standard error of the mean. Asterisks correspond to significance levels of the Spearman correlations between syndrome intensity and frequency of gluten intake according to: p ≤ 0.001 - ***, 0.001

Fig 4. Relationship between radiation-induced defecation-urgency syndrome…

Fig 4. Relationship between radiation-induced defecation-urgency syndrome and frequency of citrus fruit intake, stratified by…

Fig 4. Relationship between radiation-induced defecation-urgency syndrome and frequency of citrus fruit intake, stratified by those who have changed and those who have not changed dietary behavior after radiotherapy.
The figure depicts the relationship between frequency of citrus fruit intake (x-axis) and the intensity (factor scores) the defecation-urgency syndrome (y-axis) among long-term gynecological cancer survivors stratified according to having or not having made dietary changes after receiving radiotherapy (see the Methods section for detailed information). Red squares and green triangles denote the mean intensities of the syndromes within certain citrus intake frequency levels. Vertical black lines stretch between plus-minus the standard error of the mean. Asterisks correspond to significance levels of the Spearman correlations between syndrome intensity and frequency of citrus intake according to: p ≤ 0.001 - ***, 0.001
Similar articles
Cited by
References
    1. Khalid U, McGough C, Hackett C, Blake P, Harrington KJ, Khoo VS, et al. A modified inflammatory bowel disease questionnaire and the Vaizey Incontinence questionnaire are more sensitive measures of acute gastrointestinal toxicity during pelvic radiotherapy than RTOG grading. International journal of radiation oncology, biology, physics. 2006;64(5):1432–41. 10.1016/j.ijrobp.2005.10.007 - DOI - PubMed
    1. Resbeut M, Marteau P, Cowen D, Richaud P, Bourdin S, Dubois JB, et al. A randomized double blind placebo controlled multicenter study of mesalazine for the prevention of acute radiation enteritis. Radiotherapy and oncology: journal of the European Society for Therapeutic Radiology and Oncology. 1997;44(1):59–63. - PubMed
    1. Steineck G, Skokic V, Sjoberg F, Bull C, Alevronta E, Dunberger G, et al. Identifying radiation-induced survivorship syndromes affecting bowel health in a cohort of gynecological cancer survivors. PLoS One. 2017;12(2):e0171461 10.1371/journal.pone.0171461 - DOI - PMC - PubMed
    1. Kuku S, Fragkos C, McCormack M, Forbes A. Radiation-induced bowel injury: the impact of radiotherapy on survivorship after treatment for gynaecological cancers. Br J Cancer. 2013;109(6):1504–12. 10.1038/bjc.2013.491 - DOI - PMC - PubMed
    1. Ferreira MR, Muls A, Dearnaley DP, Andreyev HJ. Microbiota and radiation-induced bowel toxicity: lessons from inflammatory bowel disease for the radiation oncologist. Lancet Oncol. 2014;15(3):e139–47. 10.1016/S1470-2045(13)70504-7 - DOI - PubMed
Show all 56 references
Publication types
MeSH terms
Related information
Grant support
This work was supported by the Swedish Cancer Society to GS, the King Gustav V Jubilee Clinic Cancer Foundation in Göteborg, Sweden to GS and the Swedish state under the ALF agreement in Göteborg. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
[x]
Cite
Copy Download .nbib
Format: AMA APA MLA NLM

NCBI Literature Resources

MeSH PMC Bookshelf Disclaimer

The PubMed wordmark and PubMed logo are registered trademarks of the U.S. Department of Health and Human Services (HHS). Unauthorized use of these marks is strictly prohibited.

Follow NCBI
Fig 3. Relationship between intensity of excessive…
Fig 3. Relationship between intensity of excessive mucus discharge and frequency of gluten intake.
The figure depicts the relationship between frequency of gluten intake (x-axis) and the intensity (factor scores) of the radiation induced syndrome (y-axis) excessive mucus discharge among long-term gynecological cancer survivors and population controls. Red squares/green triangles denote the mean syndrome intensity within certain gluten intake frequency levels. Vertical black lines stretch between plus-minus the standard error of the mean. Asterisks correspond to significance levels of the Spearman correlations between syndrome intensity and frequency of gluten intake according to: p ≤ 0.001 - ***, 0.001

Fig 4. Relationship between radiation-induced defecation-urgency syndrome…

Fig 4. Relationship between radiation-induced defecation-urgency syndrome and frequency of citrus fruit intake, stratified by…

Fig 4. Relationship between radiation-induced defecation-urgency syndrome and frequency of citrus fruit intake, stratified by those who have changed and those who have not changed dietary behavior after radiotherapy.
The figure depicts the relationship between frequency of citrus fruit intake (x-axis) and the intensity (factor scores) the defecation-urgency syndrome (y-axis) among long-term gynecological cancer survivors stratified according to having or not having made dietary changes after receiving radiotherapy (see the Methods section for detailed information). Red squares and green triangles denote the mean intensities of the syndromes within certain citrus intake frequency levels. Vertical black lines stretch between plus-minus the standard error of the mean. Asterisks correspond to significance levels of the Spearman correlations between syndrome intensity and frequency of citrus intake according to: p ≤ 0.001 - ***, 0.001
Similar articles
Cited by
References
    1. Khalid U, McGough C, Hackett C, Blake P, Harrington KJ, Khoo VS, et al. A modified inflammatory bowel disease questionnaire and the Vaizey Incontinence questionnaire are more sensitive measures of acute gastrointestinal toxicity during pelvic radiotherapy than RTOG grading. International journal of radiation oncology, biology, physics. 2006;64(5):1432–41. 10.1016/j.ijrobp.2005.10.007 - DOI - PubMed
    1. Resbeut M, Marteau P, Cowen D, Richaud P, Bourdin S, Dubois JB, et al. A randomized double blind placebo controlled multicenter study of mesalazine for the prevention of acute radiation enteritis. Radiotherapy and oncology: journal of the European Society for Therapeutic Radiology and Oncology. 1997;44(1):59–63. - PubMed
    1. Steineck G, Skokic V, Sjoberg F, Bull C, Alevronta E, Dunberger G, et al. Identifying radiation-induced survivorship syndromes affecting bowel health in a cohort of gynecological cancer survivors. PLoS One. 2017;12(2):e0171461 10.1371/journal.pone.0171461 - DOI - PMC - PubMed
    1. Kuku S, Fragkos C, McCormack M, Forbes A. Radiation-induced bowel injury: the impact of radiotherapy on survivorship after treatment for gynaecological cancers. Br J Cancer. 2013;109(6):1504–12. 10.1038/bjc.2013.491 - DOI - PMC - PubMed
    1. Ferreira MR, Muls A, Dearnaley DP, Andreyev HJ. Microbiota and radiation-induced bowel toxicity: lessons from inflammatory bowel disease for the radiation oncologist. Lancet Oncol. 2014;15(3):e139–47. 10.1016/S1470-2045(13)70504-7 - DOI - PubMed
Show all 56 references
Publication types
MeSH terms
Related information
Grant support
This work was supported by the Swedish Cancer Society to GS, the King Gustav V Jubilee Clinic Cancer Foundation in Göteborg, Sweden to GS and the Swedish state under the ALF agreement in Göteborg. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
[x]
Cite
Copy Download .nbib
Format: AMA APA MLA NLM
Fig 4. Relationship between radiation-induced defecation-urgency syndrome…
Fig 4. Relationship between radiation-induced defecation-urgency syndrome and frequency of citrus fruit intake, stratified by those who have changed and those who have not changed dietary behavior after radiotherapy.
The figure depicts the relationship between frequency of citrus fruit intake (x-axis) and the intensity (factor scores) the defecation-urgency syndrome (y-axis) among long-term gynecological cancer survivors stratified according to having or not having made dietary changes after receiving radiotherapy (see the Methods section for detailed information). Red squares and green triangles denote the mean intensities of the syndromes within certain citrus intake frequency levels. Vertical black lines stretch between plus-minus the standard error of the mean. Asterisks correspond to significance levels of the Spearman correlations between syndrome intensity and frequency of citrus intake according to: p ≤ 0.001 - ***, 0.001

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    1. Resbeut M, Marteau P, Cowen D, Richaud P, Bourdin S, Dubois JB, et al. A randomized double blind placebo controlled multicenter study of mesalazine for the prevention of acute radiation enteritis. Radiotherapy and oncology: journal of the European Society for Therapeutic Radiology and Oncology. 1997;44(1):59–63.
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Source: PubMed

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