Structural and functional parameters of erythrocytes as predictors of unfavorable outcome in patients with colorectal cancer

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Abstract

Aim. Identification the characteristics of fatty acids (FAs) in erythrocyte membranes and in blood serum, as well as the electrical and viscoelastic parameters of erythrocytes to assess their ability to be predictors of an unfavorable outcome in patients with colorectal cancer (CRC).

Materials and methods. 112 people with an average age of 63.1 ± 9.5 years (62 men, 50 women) with CRC of stages I–IV were examined. The patients were divided into 2 groups depending on the outcome of the disease after 6 years of follow-up: group 1 – with stabilization of the disease (n = 55), group 2 (n = 57) – with an unfavorable outcome. The FA composition of erythrocyte membranes and blood serum was studied using gas chromatography/mass spectrometry, a system based on three Agilent 7000B quadrupoles (USA). The electrical and viscoelastic parameters of erythrocytes were studied using the method of dielectrophoresis.

Results. An unfavorable outcome in patients with CRC is associated with elevated levels of docosapentaenoic acid (C22:5n-3) (p = 0.0003), docosahexaenoic acid (C22:6n-3) (p = 0.001), docosathetraenoic acid (C22:4n-6) (p = 0.004), and total omega-3 polyunsaturated fatty acids (PUFA) (p = 0.0004) in erythrocyte membranes, eicosadienoic acid (C20:2 n-6) in erythrocyte membranes (p = 0.03) and blood serum (p = 0.01), and, conversely, reduced levels of ratios saturated fatty acids (SFA)/PUFA (p = 0.004), SFA / unsaturated fatty acids (USFA) (p = 0.01) and concentrations of myristic FA (C14:0) (p = 0.03) in erythrocyte membranes, as well as with a number of changes in electrical, viscoelastic parameters of red blood cells: with increased hemolysis of red blood cells at high frequencies (106 Hz – p = 0.0006 and 5 × 105 Hz – p = 0.046), increased aggregation indices at low frequencies (105 Hz – p = 0.04 and 5 × 104 Hz – p = 0.047), as well as a shift in the crossover frequency to the high frequency range (p = 0.036). In patients with stages 1–2 of CRC, omega-6 PUFAs, eicosadienoic acid C20:2n-6 (p = 0.006), docosatetraenoic acid C22:4n-6 (p = 0.012), were of the greatest importance for differentiating disease outcomes, while total content omega-3 PUFAs in erythrocyte membranes (p = 0.0129), docosahexaenoic acid C22:6 n-3 (p = 0.0169), total content (C20:5n-3+C22:6n-3) in erythrocyte membranes (p = 0.0198), docosapentaenoic acid C22:5 n-3 (p = 0.022) were slightly less important. As in the general group of patients with CRC, the degree of hemolysis at a frequency of 106 Hz was a predictor of an unfavorable outcome in people with early stages of the oncological process. ROC analysis revealed a high potential of palmitic acid in erythrocyte membranes to predict an unfavorable CRC outcome (AUC 0.786, 95% confidence interval 0.638–0.901, sensitivity 84.4%, specificity 68.2%). The diagnostic model, which included five parameters – erythrocyte levels C16:0, ratio SFA/PUFA, total USFA, total PUFA, and serum levels C20:2n-6, had an AUC of 0.663 (95% confidence interval 0.483–0.801) with the highest sensitivity of 85.2%, but not high specificity of 60.1% for predicting an unfavorable outcome in CRC.

Conclusion. Fatty acids of erythrocyte membranes, blood serum, electrical, and viscoelastic parameters of erythrocytes should be considered as promising biomarker predictors in patients with CRC that require further study.

About the authors

Margarita V. Kruchinina

Research Institute of Internal and Preventive Medicine; Novosibirsk State Medical University

Author for correspondence.
Email: kruchmargo@yandex.ru
ORCID iD: 0000-0003-0077-3823

д-р мед. наук, проф., зав. лаб. гастроэнтерологии, вед. науч. сот. лаб. гастроэнтерологии; проф. каф. пропедевтики внутренних болезней

Russian Federation, Novosibirsk; Novosibirsk

Marina F. Osipenko

Novosibirsk State Medical University

Email: kruchmargo@yandex.ru
ORCID iD: 0000-0002-5156-2842

д-р мед. наук, проф., зав. каф. пропедевтики внутренних болезней

Russian Federation, Novosibirsk

Andrey A. Gromov

Research Institute of Internal and Preventive Medicine

Email: kruchmargo@yandex.ru
ORCID iD: 0000-0001-9254-4192

канд. мед. наук, ст. науч. сотр. лаб. клинических биохимических и гормональных исследований терапевтических заболеваний, руководитель Центра профилактики тромбозов

Russian Federation, Novosibirsk

Andrey V. Starikov

Novosibirsk Regional Oncology Dispensary

Email: kruchmargo@yandex.ru
ORCID iD: 0009-0009-6776-3401

врач-онколог

Russian Federation, Novosibirsk

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2. Fig. 1. Normalization of the levels of electrical and viscoelastic parameters of erythrocytes, the content of fatty acids in erythrocyte membranes, and blood serum (on the left – levels of indicators before normalization, on the right – after normalization).

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3. Fig. 2. Principal component analysis (PCA) to distinguish patients with stage I–II CRC with poor outcome and stable outcome.

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4. Fig. 3. ROC curves of the models for establishing prognosis in colorectal cancer: a – for erythrocyte C16:0 – AUC 0.786 (95% CI 0.638–0.901); b – for serum C20:2n-6 – AUC 0.716 (95% CI 0.57–0.853); c – for erythrocyte C22:4n-6 – AUC 0.697 (95% CI 0.528–0.838); d – SFA/PUFA in erythrocyte membranes –AUC 0.689 (95% CI 0.53–0.841); e – list of diagnostic panels including different numbers of fatty acids, with AUC from 0.587 to 0.663; f – A diagnostic model including red blood cell levels of C16:0, SFA/PUFA, SFA, PUFA and serum level of C20:2n-6 [AUC 0.663 (95% CI 0.483–0.801)].

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5. Fig. 4. The contribution of erythrocyte membrane fatty acid levels and blood serum to distinguishing patients with stage 1–2 CRC with unfavorable outcome and stabilization.

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Согласие на обработку персональных данных с помощью сервиса «Яндекс.Метрика»

1. Я (далее – «Пользователь» или «Субъект персональных данных»), осуществляя использование сайта https://journals.rcsi.science/ (далее – «Сайт»), подтверждая свою полную дееспособность даю согласие на обработку персональных данных с использованием средств автоматизации Оператору - федеральному государственному бюджетному учреждению «Российский центр научной информации» (РЦНИ), далее – «Оператор», расположенному по адресу: 119991, г. Москва, Ленинский просп., д.32А, со следующими условиями.

2. Категории обрабатываемых данных: файлы «cookies» (куки-файлы). Файлы «cookie» – это небольшой текстовый файл, который веб-сервер может хранить в браузере Пользователя. Данные файлы веб-сервер загружает на устройство Пользователя при посещении им Сайта. При каждом следующем посещении Пользователем Сайта «cookie» файлы отправляются на Сайт Оператора. Данные файлы позволяют Сайту распознавать устройство Пользователя. Содержимое такого файла может как относиться, так и не относиться к персональным данным, в зависимости от того, содержит ли такой файл персональные данные или содержит обезличенные технические данные.

3. Цель обработки персональных данных: анализ пользовательской активности с помощью сервиса «Яндекс.Метрика».

4. Категории субъектов персональных данных: все Пользователи Сайта, которые дали согласие на обработку файлов «cookie».

5. Способы обработки: сбор, запись, систематизация, накопление, хранение, уточнение (обновление, изменение), извлечение, использование, передача (доступ, предоставление), блокирование, удаление, уничтожение персональных данных.

6. Срок обработки и хранения: до получения от Субъекта персональных данных требования о прекращении обработки/отзыва согласия.

7. Способ отзыва: заявление об отзыве в письменном виде путём его направления на адрес электронной почты Оператора: info@rcsi.science или путем письменного обращения по юридическому адресу: 119991, г. Москва, Ленинский просп., д.32А

8. Субъект персональных данных вправе запретить своему оборудованию прием этих данных или ограничить прием этих данных. При отказе от получения таких данных или при ограничении приема данных некоторые функции Сайта могут работать некорректно. Субъект персональных данных обязуется сам настроить свое оборудование таким способом, чтобы оно обеспечивало адекватный его желаниям режим работы и уровень защиты данных файлов «cookie», Оператор не предоставляет технологических и правовых консультаций на темы подобного характера.

9. Порядок уничтожения персональных данных при достижении цели их обработки или при наступлении иных законных оснований определяется Оператором в соответствии с законодательством Российской Федерации.

10. Я согласен/согласна квалифицировать в качестве своей простой электронной подписи под настоящим Согласием и под Политикой обработки персональных данных выполнение мною следующего действия на сайте: https://journals.rcsi.science/ нажатие мною на интерфейсе с текстом: «Сайт использует сервис «Яндекс.Метрика» (который использует файлы «cookie») на элемент с текстом «Принять и продолжить».