Oxidative stability of lutein on exposure to varied extrinsic factors

Ishani Bhat; Nimmy Mol Jose; Bangera Sheshappa Mamatha

doi:10.1007/s13197-022-05430-3

. 2022 Apr 15;60(3):987–995. doi: 10.1007/s13197-022-05430-3

Oxidative stability of lutein on exposure to varied extrinsic factors

Ishani Bhat ¹, Nimmy Mol Jose ¹, Bangera Sheshappa Mamatha ^1,^✉

PMCID: PMC9998772 PMID: 36908359

Abstract

Pre-processing treatments performed on lutein sources can cause it to degrade, generating superfluous metabolites and lowering lutein’s bioactivity. However, evidences suggesting extent of reduction in functional stability of lutein on exposure to such treatment conditions are nil. This study is first of its kind, where we attempted to gain clarity on the extent of degradation caused by the changes in temperature (40–100 °C), pH (2–8) and duration of such treatments. Increase (3.9 folds) in lutein loss within an hour at 40 °C occurred when pH was lowered from 8 to 2. Increase (1.7 folds) in lutein loss at neutral pH and 40 °C occurred when duration of exposure was increased from 1 to 4 h. Besides, lutein loss significantly increased on rising the temperature by every 10 °C. The functional stability of lutein in relation to its degradation was also studied by monitoring its radical scavenging activity. While lutein is highly unstable, lutein structure and its respective bioactivity can be significantly (p < 0.05) retained (< 12.44% and > 54.87% respectively) by maintaining the operating conditions at higher pH (7–8) and lower temperatures (40–50 °C) for a short period of time (< 1 h).

Supplementary Information

The online version contains supplementary material available at 10.1007/s13197-022-05430-3.

Keywords: Antioxidant activity, Functional stability, Lutein, Nutraceutical, Oxidative degradation, Xanthophyll carotenoid

Introduction

Lutein belongs to the class of xanthophyll carotenoids which can be sourced in yellow-orange fruits and green vegetables. Lutein is extremely hydrophobic as seen by the nature of its structure, β,ε-carotene-3,3-diol (C₄₀H₅₆O₂) comprising isoprene backbone and double bonds. Often, the structure can exist in its original all-trans configuration (E conformation) or cis configuration (Z conformation) as its stereoisomer zeaxanthin. Besides, free electron movement in these bonds allow them to absorb blue light in the range of 450–485 nm of the visible spectrum (Mora-Gutierrez et al. 2018; Yi et al. 2016). This enables lutein and zeaxanthin to exhibit strong antioxidant activity as a macular pigment in the human eye. Although human body does not encompass mechanisms to synthesize lutein, its benefits can be availed by dietary consumption of photosynthetic sources. Oral consumption of lutein is associated with prevention of several life-threatening diseases including many classes of cancers (Bhat et al. 2020). However, the bioactivity of the compound depends on the amount of original compound that reaches the target site and is available for action which in turn depends on its bioaccessibility (Bhat and Mamatha 2021). The determinants of lutein oral bioavailability are abbreviated as SLAMENGI, which includes species of the carotenoid, linkage of the molecules, amount of carotenoid consumed, matrix surrounding the carotenoid, effectors of absorption and bioconversion, nutrition status of the host, genetic variations of the host, and mathematical interactions as the factors (Castenmiller and West 1998). Prior to oral consumption, the sources are processed by heat, pressure and abruption for improved palatability. Exposure to oxygen, changes in the moisture content and pH during the processing steps forces lutein to undergo series of changes that may modify its chemical structure (Bhat et al. 2021b; Gouveia and Empis 2003). Such modifications may result in formation of lower molecular weight compounds that are colorless (Boon et al. 2010; Cheng et al. 2019). Moreover, cis isomer of lutein is thermodynamically less stable than its original all-trans form (Yang et al. 2018). Sustaining the stability of lutein during processing and digestion is important to allow maximum bioaccessibility and intestinal absorption. Although few reports have thrown light upon the possible factors affecting structural stability of lutein, modulation of its antioxidant activity in accordance with its structural changes is yet not clearly understood. Identifying the grey area to be explored, we attempted a fresh approach to study the functional stability of lutein as affected by processing conditions. This study is first of its kind where a time dependent experimental setup was designed to decipher the effect of varying pH and processing temperatures on the structural integrity and bioactivity of lutein.

Materials and methods

Chemicals

Lutein standard was purchased from Sigma-Aldrich Chemicals Pvt Ltd (USA). Solvents used for extraction, purification and analysis such as hexane, acetonitrile, methanol, and dichloromethane were of HPLC grade purchased from Himedia (Bengaluru, India). Other chemicals used for the study were of analytical grade.

Lutein extraction and purification

Marigold flowers were used for lutein extraction and purification according to the method prescribed by Bhat et al. (2021a). Marigold flowers were macerated with ice-cold acetone, saponified with 30% methanolic KOH (1:4) and separated using hexane. The carotenoids were separated on an open silica column (120–60) and lutein was eluted using acetonitrile / methanol / dichloromethane in the ratio 3:1:1 (v/v/v). Lutein standard was used to compare the purity of eluted lutein by HPLC. To avoid photoisomerization and oxidation of lutein, handling and purifying procedures were carried out under dull yellow light.

Experimental design

The experimental setup was designed as shown in Fig. 1 under closed conditions in the absence of light. Purified lutein (3 µg, as standardized by preliminary trials) was completely dissolved in DMSO (10 µL) prior to mixing with buffers (1:20, v/v) of specific pH. The buffers were prepared using appropriate proportions of salts for accurate pH as prescribed by Torskangerpoll and Aderson (2005). The samples were exposed to specific pH conditions (2, 3, 4, 5, 6, 7 and 8) and temperatures (40, 50, 60, 70, 80, 90 and 100 °C). Samples were separately exposed for a definite time interval and were withdrawn at specific time intervals (1, 2, 3, and 4 h). No sample was disturbed in between the exposure time and the volume was kept constant. Post exposure, lutein was extracted and estimated by HPLC.

Lutein extraction after exposure

Samples were processed immediately on completion of exposure to different temperatures and pHs for specified time. Lutein was extracted from samples Bhat et al. (2021a) using dichloromethane:methanol:hexane in the ratio 2:2:4:3 (v/v/v/v). The mixture was vortexed (1 min), centrifuged (3000 rpm, 5 min) and upper layer of hexane was collected. Repeated extraction was performed with the lower aqueous layer using dichloromethane:hexane (2:3 v/v) and centrifugation (1000 ×g, 5 min) at room temperature. The upper hexane layer was collected, pooled and dried over a stream of nitrogen. The samples were redissolved in a known amount of mobile phase and analyzed by HPLC.

HPLC analysis

The samples were analyzed on C-18 (ODS) column (4.6 × 250 mm, 5 µm pore size) according to the method prescribed by Bhat et al. (2021a). A 3:1:1 (v/v/v) mixture of acetonitrile:methanol:dichloromethane was used as mobile phase. All the samples were analyzed in isocratic condition with 1 mL/min flow rate in Waters HPLC system equipped with photodiode array detector (450 nm).

Antioxidant activity

Free radical scavenging activity of lutein and its oxidation products were measured using DPPH assay according to the method prescribed by Rai et al. (2017). DPPH (200 µl) was added to an aliquot of the sample (20 µL) and incubated in dark conditions at room temperature (30 min) following which absorbance was measured at 517 nm using a spectrophotometer (Thermoscientific Multiscan Sky). The radical scavenging activity was calculated by applying the formula:

S c a v e n g i n g e f f e c t (%) = \{1 - [(A_{sample} - A_{blank}) / A_{control}]\}

where A_sample is absorbance of sample, A_blank is absorbance of blank and A_control is absorbance of control.

Statistical analysis

The values were reported as mean ± SD (n = 3). The results were tested by three-way ANOVA and Tukey’s multiple comparison tests. The difference between the means was considered to be statistically significant at p ≤ 0.05.

Results and discussion

Purification of lutein

The lutein prepared from marigold flowers showed the retention time and λ_max to be 4.04 min and 445 nm respectively. This was comparable to the reference standard (Fig. 2). Moreover, the prepared lutein had 97% purity. Since the use of prepared lutein on a comparison against the reference standard has been reported earlier, it was used for further experiments (Bhat et al. 2021a).

Fig. 2 — Chromatograms of prepared lutein (A) in comparison to reference standard (B)

Effect of pH on lutein

Severe changes in the pH (below 4 or above 8) is known to initiate isomerization (cis/trans) of lutein (Boon et al. 2010). The thermodynamic instability of the isomer can further fuel formation of lutein degradative compounds. In this study, a range of pH (2–8) was chosen to mimic food matrices and environment that lutein would be exposed to. The range of pH was chosen since most of the beverages, milk, milk substitutes and other such lutein sources are well within this range. Irrespective of the temperature and duration of exposure lutein was unstable at lower pH (Fig. 3). To understand the effect of pH alone irrespective of temperature and duration of exposure, values at lowest temperature (40 °C) and shortest duration of exposure (1 h) were monitored. While exposure to pH 8 caused 12.44% loss, exposure to pH 2 at same conditions caused 48.89% loss (Table 1). Around the neutral pH (8–6) only 12–20% of lutein loss was observed. The percentage loss of lutein was inversely related to pH where, lowering the pH caused higher degradation. A similar study also reported hindered stability of lutein at pH 4–5 (Boon et al. 2010). Moreover, a sudden significant (p < 0.5) increase in the loss of lutein from 29 to 48.89% occurred on changing the pH from 3 to 2. Concordant to the results of this study, lutein was reported to be relatively stable at higher pH precisely at pH 8 (Boon et al. 2010). At lower temperatures (40–50 °C), there was no significant changes (p < 0.5) between pH 7 and 8. At moderate temperature (60 °C), there was no significant changes (p < 0.5) in the pH ranging from 4 to 6. Whereas, at higher temperatures (70–80 °C) there was no significant changes (p < 0.5) between pH 2 and 4. Protonation of C atoms present in the conjugated double bonds of the carotenoid structure often accelerates its isomerization and degradation (Gumus et al. 2016). However, hydroxyl groups in lutein structure alter the protonation of C atoms to provide higher stability counter to pH variations. Although variation in the pH caused significant oxidative degradation in lutein, it was jointly influenced by temperature and duration of exposure.

Fig. 3 — Stability of lutein on exposure to temperatures ranging from 40 to 100 °C for 1–4 h at A pH 2, B pH 3, C pH 4, D pH 5, E pH 6, F pH 7 and G pH 8

Table 1.

Time dependent oxidative degradation of lutein on exposure to varied temperatures and pH conditions

Temperature (°C)	Time (h)	Oxidative degradation of lutein (%)
Temperature (°C)	Time (h)	pH 2	pH 3	pH 4	pH 5	pH 6	pH 7	pH 8
40	0	0.00^a/α/A	0.00^a/α/A	0.00^a/α/A	0.00^a/α/A	0.00^a/α/A	0.00^a/α/A	0.00^a/α/A
	1	48.89 ± 5.10^e/β/B	29.00 ± 0.67^d/β/B	26.56 ± 0.69^cd/β/B	23.78 ± 1.02^bc/β/B	20.67 ± 1.00^b/β/B	15.22 ± 1.90^a/β/B	12.44 ± 1.58^a/β/B
	2	60.67 ± 3.21^f/γ/CD	32.33 ± 0.58^e/β/B	29.33 ± 2.33^de/β/B	26.33 ± 2.40^cd/β/B	23.00 ± 1.45^bc/βγ/BC	18.44 ± 1.71^ab/βγ/BC	15.33 ± 1.45^a/β/B
	3	64.44 ± 1.71^e/γ/D	38.89 ± 1.26^d/γ/C	38.22 ± 3.10^d/γ/C	33.22 ± 3.01^c/γ/C	26.22 ± 1.64^b/γ/C	22.56 ± 1.39^ab/γ/CD	19.67 ± 0.67^a/γ/CDE
	4	69.11 ± 1.58^f/δ/E	59.56 ± 2.50^e/δ/D	53.78 ± 2.67^d/δ/E	41.22 ± 1.84^c/δ/E	35.89 ± 3.02^b/δ/D	27.11 ± 0.84^a/δ/DE	24.11 ± 1.39^a/δ/EFG
50	0	0.00^a/α/A	0.00^a/α/A	0.00^a/α/A	0.00^a/α/A	0.00^a/α/A	0.00^a/α/A	0.00^a/α/A
	1	58.11 ± 3.34^e/β/C	30.56 ± 1.17^d/β/B	29.00 ± 1.53^cd/β/B	24.78 ± 0.96^bc/β/B	22.56 ± 2.55^b/β/BC	16.89 ± 0.51^a/β/B	15.56 ± 0.51^a/β/BC
	2	65.44 ± 2.04^d/γ/DE	37.78 ± 1.95^c/γ/C	29.11 ± 1.58^b/β/B	27.33 ± 2.33^b/β/B	25.11 ± 1.17^b/βγ/BC	19.67 ± 2.33^a/βγ/BC	17.00 ± 0.67^a/β/BC
	3	72.33 ± 3.71^f/δ/E	55.89 ± 1.84^e/δ/D	40.67 ± 2.08^d/γ/C	35.67 ± 2.00^c/γ/CD	27.44 ± 1.39^b/γ/C	23.11 ± 2.83^ab/γ/CD	19.00 ± 1.86^a/β/CD
	4	85.44 ± 1.95^e/ε/FG	66.33 ± 1.33^d/ε/E	47.67 ± 3.06^c/δ/D	43.89 ± 1.02^b/δ/E	39.56 ± 1.17^b/δ/D	29.56 ± 1.64^a/δ/E	27.44 ± 1.71^a/γ/FG
60	0	0.00^a/α/A	0.00^a/α/A	0.00^a/α/A	0.00^a/α/A	0.00^a/α/A	0.00^a/α/A	0.00^a/α/A
	1	82.11 ± 3.56^d/β/F	65.78 ± 1.68^c/β/E	38.22 ± 3.79^b/β/C	39.44 ± 4.82^b/β/DE	37.22 ± 1.39^b/β/D	29.22 ± 1.39^a/β/E	23.67 ± 0.67^a/β/DEF
	2	90.22 ± 1.58^e/γ/G	72.00 ± 3.79^d/γ/F	58.56 ± 2.52^c/γ/E	55.33 ± 3.84^c/γ/F	56.11 ± 2.59^c/γ/E	38.22 ± 4.07^b/γ/F	29.33 ± 2.00^a/β/G
	3	94.22 ± 1.35^f/γ/GH	76.56 ± 2.22^e/γδ/F	67.78 ± 2.36^d/δ/G	63.56 ± 3.42^cd/δ/G	58.22 ± 1.84^c/γ/E	48.22 ± 3.75^b/δ/G	37.22 ± 2.80^a/γ/H
	4	96.11 ± 1.02^e/γ/HI	82.44 ± 3.02^d/δ/G	76.89 ± 2.41^cd/ε/	75.22 ± 4.22^c/ε/	71.00 ± 1.86^c/δ/G	63.11 ± 2.69^b/ε/I	44.78 ± 4.35^a/δ/I
70	0	0.00^a/α/A	0.00^a/α/A	0.00^a/α/A	0.00^a/α/A	0.00^a/α/A	0.00^a/α/A	0.00^a/α/A
	1	97.00 ± 0.67^e/β/HI	87.89 ± 2.04^d/β/H	64.56 ± 1.39^d/β/F	62.78 ± 1.02^c/β/G	59.11 ± 1.17^b/β/EF	54.67 ± 2.08^a/β/H	51.22 ± 2.22^a/β/J
	2	99.00 ± 0.33^d/β/HI	95.89 ± 1.17^d/γ/I	71.44 ± 3.02^d/γ/H	69.11 ± 1.35^c/γ/H	64.44 ± 2.99^b/γ/F	59.11 ± 1.35^a/γ/HI	55.78 ± 1.35^a/γ/JK
	3	99.81 ± 0.08^d/β/I	97.00 ± 0.67^d/γ/I	85.89 ± 3.29^d/γ/H	77.89 ± 2.52^c/δ/I	71.89 ± 2.52^b/δ/G	61.00 ± 0.88^a/γ/I	58.78 ± 1.84^a/γ/K
	4	99.97 ± 0.03^e/β/HI	99.00 ± 0.33^e/γ/I	94.00 ± 1.53^e/γ/H	87.33 ± 1.00^d/ε/J	83.11 ± 2.46^c/ε/H	71.67 ± 2.91^b/δ/J	64.33 ± 1.53^a/δ/L
80	0	0.00^a/α/A	0.00^a/α/A	0.00^a/α/A	0.00^a/α/A	0.00^a/α/A	0.00^a/α/A	0.00^a/α/A
	1	100.00^d/β/HI	99.97 ± 0.03^d/β/I	99.78 ± 0.04^d/β/H	99.56 ± 0.19^d/β/K	96.89 ± 0.51^c/β/I	87.11 ± 2.22^b/β/K	84.00 ± 2.96^a/β/M
	2	100.00^c/β/HI	100.00^c/β/I	99.98 ± 0.02^c/β/H	99.74 ± 0.04^c/β/K	99.57 ± 0.20^c/γ/I	95.33 ± 1.45^b/γ/L	90.89 ± 2.83^a/γ/N
	3	100.00^b/β/HI	100.00^b/β/I	100.00^b/β/H	99.94 ± 0.05^b/β/K	99.88 ± 0.13^b/γ/I	98.33 ± 0.88^b/δ/L	93.56 ± 1.07^a/δ/N
	4	100.00^a/β/HI	100.00^a/β/I	100.00^a/β/H	100.00^a/β/K	100.00^a/γ/I	99.74 ± 0.04^a/δ/L	99.72 ± 0.07^a/ε/O

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Values are mean ± SD (n = 3); Values within the same row between the pH, which do not share similar letters in the superscript are significantly different (p ≤ 0.05) as determined by three-way ANOVA and Tukey’s multiple comparison test. Significantly different (p ≤ 0.05) values within the same column are indicated by dissimilar capitalized letters and the same for every temperature are indicated by dissimilar Greek letters in the superscript

Effect of temperature on lutein

Thermal processing is most commonly practised in food industries, restaurants and households to not only improve the edibility but also enhance its palatability. Procedures like blanching, pasteurizing, cooking, canning, frying, drying, roasting and such others that use heat energy may seem simple to serve the purpose. However, they rupture the cell walls and make lutein more bioaccessible, exposing lutein to the environment, which can accelerate its oxidative degradation. A similar pattern was observed in this study concerning the temperature of exposure (Fig. 3). To understand the effect of temperature alone irrespective of pH and duration of exposure, values at neutral pH (7) and shortest duration of exposure (1 h) were monitored. Study results clearly indicated direct relation between processing temperature and lutein degradation. Exposure to temperatures as low as 40 and 50 °C caused 15.22 and 16.89% lutein loss, which was insignificantly different. With increasing temperatures more and more lutein loss occurred, which reached up to 87.11% at 80 °C. Temperatures beyond 80 °C caused complete degradation of lutein (100%). At pH 2, complete degradation was observed at 70 °C. These results precisely support the hypothesis of this study that rise in the temperatures accelerates oxidative degradation of lutein (Table 1). On the other hand, heat can cause rupture of cellular matrix to liberate lutein and improve its bioaccessibility (Boon et al. 2010). Few reports suggest short period heat treatment in corn, onion, broccoli, capsicum, pistachios for improving lutein release from the matrix (Eriksen et al. 2016; Mamatha et al. 2012; Ranganathan et al. 2014). However, the action of heat on food matrix and nature of the matrix decides the speed of lutein release (Komuro et al. 2017). Following its release, lutein degradation can occur easily on exposure to high temperatures (Gutiérrez-Uribe et al. 2014; Shen et al. 2015). This is well reflected in this study, where lutein was extracted and subjected to heat treatment (Table 1). However, the duration of exposure is a subject of concern.

Duration of exposure

Although pH and temperature affect stability of lutein independently, it is largely modulated by the duration of exposure. At all the pH and temperatures studied, prolonged exposure caused greater instability and degradation of the compound (Fig. 3). For example, at neutral pH 7 and lowest temperature (40 °C), from 0–1 h only 15.22% lutein loss was observed. By the end of 4 h, 27.11% lutein loss occurred. This pattern was observed for all other temperatures at respective pH. Oxidative degradation occurring at most of the temperatures and pH were significantly differing (p < 0.5) between time intervals designed in the study (Table 1). Lutein is found in photosynthetic sources and is usually embedded well within the chloroplast. During the food processing, high temperature treatments and pH of the medium disrupts the cellular integrity, which exposes lutein to stressful environments. This is reflected in the results of this study (Table 1), where minimal losses in the 1st h rises to significant oxidative degradation on prolonged exposure. Additionally, lutein degradation in food source is dependent on its initial release from the matrix whose degradation is what follows. Although few reports suggest short time heat treatment as discussed in the previous section, longer duration treatment can be detrimental to the compound. A study conducted on assessing bioaccessibility of lutein from spinach reported reduction in lutein content on boiling for 90 min in comparison to 8 min (Chung et al. 2019). The authors extended their results to suggest lutein degradation at given temperature and environmental conditions is time-dependent. Therefore, slower release can be achieved by reduced processing time, which can prospectively reduce lutein degradation (Sánchez et al. 2014).

Functional stability of lutein

During the last few decades, lutein has been explored as a significant element in preventing Age-related Macular Degeneration (AMD) and enhancing eye health. Primarily, the structure of lutein allows it to quench singlet oxygen and exhibit antioxidant property (Dall’Osto et al. 2017). Recently, lutein has been associated with prevention of neurodegenerative disorders due to its protective action against oxidation of omega-3 fatty acids (Bhat et al. 2021b; Nolan et al. 2014; Renzi-hammond et al. 2017). Besides, it can induce other antioxidant enzymes, lower serum cholesterol, reduce lipid peroxidation and oxidative stress (Fatani et al. 2015; Kamoshita et al. 2016; Murillo et al. 2016; Qiu et al. 2015). However, the key to this bioactivity is the free electron movement among the conjugated double bonds in the isoprene backbone of its structure. Disruption of this structure lowers the ability of lutein to function as an antioxidant. In this study, Radical Scavenging Activity (RSA) of lutein on time-dependent exposure to varied temperatures and pH conditions was studied. RSA of lutein reduced with increasing oxidative degradation (Table 1 and 2). At neutral pH and 40 °C the RSA significantly reduced (p < 0.5) from 63.52 to 53.53% within the 1st hour. Increasing temperatures significantly (p < 0.5) accelerated the RSA reduction. While there was no RSA detected beyond 80 °C for all the pH, at pH 2 RSA was not detected beyond 70 °C. Similar to oxidative degradation, RSA reduced significantly (p < 0.5) with reducing pH. Moreover, duration of exposure controlled most of the differences in the RSA. Longer duration of exposure caused greater reduction in RSA. For example, at neutral pH and 70 °C, RSA was significantly reduced (p < 0.5) from 63.52 to 33.75% within 1^st hour. Further, within 4 h the RSA was significantly reduced (p < 0.5) to 21.56%. Lutein content is directly proportional to the RSA exhibited under specific conditions. Although few studies report the antioxidant activity of lutein, reports on the effect of temperature or pH on bioactivity of lutein is nil. This is the first study to report the functional stability of lutein with regard to differences in the temperature and pH conditions. This study does not discuss the effects of light on the stability of lutein as the complete study was performed in the absence of light. Nonetheless, this study has successfully deciphered the effects of processing temperatures in a range of pH for specific time periods. The results of this study are suggestive of significantly retaining lutein structure and its respective bioactivity during processing at higher pH (7–8) and lower temperatures (40–50 °C) for a short period of time (< 1 h). Achieving lutein levels in the targeted organs post oral consumption is dependent on the conditions lutein is exposed to both before and after consumption. Maintaining the oxidative stability of lutein is however difficult in the latter. Prior to consumption, cooking of vegetables can be replaced by blanching for shorter periods to reduce oxidative degradation of lutein. During cooking, maintaining the pH of the cooking medium above 6 can substantially help in lutein stability.

Table 2.

Changes in the radical scavenging activity of lutein on exposure to varied temperatures and pH conditions

pH conditions	Time (h)	Radical scavenging activity (%)
pH conditions	Time (h)	40 °C	50 °C	60 °C	70 °C	80 °C
2	0	63.52 ± 0.99^a/α/O	63.52 ± 0.99^a/α/M	63.52 ± 0.99^a/α/J	63.52 ± 0.99^a/α/K	63.52 ± 0.99^a/α/E
	1	33.93 ± 1.59^e/β/BC	29.95 ± 0.83^d/β/C	16.13 ± 0.12^c/β/C	5.55 ± 0.52^b/β/B	0.00^a/β/A
	2	31.26 ± 0.66^e/γ/B	21.00 ± 0.09^d/γ/B	9.38 ± 0.22^c/γ/B	1.98 ± 0.49^b/γ/A	0.00^a/β/A
	3	21.35 ± 0.58^d/δ/A	19.40 ± 0.53^c/δ/B	7.05 ± 0.59^b/δ/AB	1.35 ± 0.27^a/γ/A	0.00^a/β/A
	4	20.70 ± 0.53^d/δ/A	16.46 ± 0.48^c/ε/A	6.15 ± 0.64^b/δ/A	0.66 ± 0.57^a/γ/A	0.00^a/β/A
3	0	63.52 ± 0.99^a/α/O	63.52 ± 0.99^a/α/M	63.52 ± 0.99^a/α/J	63.52 ± 0.99^a/α/K	63.52 ± 0.99^a/α/E
	1	41.51 ± 1.14^e/β/GHI	39.05 ± 0.33^d/β/EFG	31.40 ± 0.61^c/β/F	19.46 ± 0.48^b/β/E	0.72 ± 0.63^a/β/A
	2	37.36 ± 1.63^d/γ/DE	36.32 ± 0.69^d/γ/D	26.78 ± 0.98^c/γ/E	8.05 ± 0.78^b/γ/BC	0.00^a/β/A
	3	35.26 ± 0.43^e/δ/CD	30.28 ± 1.06^d/δ/C	20.45 ± 0.42^c/δ/D	6.48 ± 1.02^b/γ/B	0.00^a/β/A
	4	31.93 ± 0.88^e/ε/B	21.58 ± 0.99^d/ε/B	15.78 ± 1.26^c/ε/C	2.15 ± 0.61^b/δ/A	0.00^a/β/A
4	0	63.52 ± 0.99^a/α/O	63.52 ± 0.99^a/α/M	63.52 ± 0.99^a/α/J	63.52 ± 0.99^a/α/K	63.52 ± 0.99^a/α/E
	1	42.84 ± 0.18^e/β/HI	40.45 ± 0.54^d/β/FGH	30.40 ± 0.53^c/β/F	19.46 ± 0.48^b/β/E	4.57 ± 0.59^a/β/B
	2	39.03 ± 1.00^d/γ/FG	38.95 ± 0.20^d/β/DEF	26.78 ± 0.98^c/γ/E	13.51 ± 1.54^b/γ/D	1.46 ± 0.67^a/γ/A
	3	37.26 ± 1.64^d/δ/DE	36.28 ± 0.70^d/γ/DE	20.45 ± 0.42^c/δ/D	9.68 ± 0.29^b/δ/C	0.00^a/γ/A
	4	32.26 ± 1.09^d/ε/B	31.95 ± 0.84^d/δ/C	15.78 ± 1.26^c/ε/C	8.15 ± 0.61^b/δ/BC	0.00^a/γ/A
5	0	63.52 ± 0.99^a/α/O	63.52 ± 0.99^a/α/M	63.52 ± 0.99^a/α/J	63.52 ± 0.99^a/α/K	63.52 ± 0.99^a/α/E
	1	47.47 ± 0.64^e/β/J	44.93 ± 0.84^d/β/IJ	36.74 ± 0.55^c/β/G	23.26 ± 1.72^b/β/F	4.61 ± 0.55^a/β/BC
	2	43.84 ± 0.18^e/γ/I	40.55 ± 0.46^d/γ/FGH	30.43 ± 0.59^c/γ/F	20.13 ± 1.07^b/γ/E	1.86 ± 0.60^a/γ/AB
	3	40.36 ± 1.55^d/δ/FGH	39.95 ± 1.02^d/γ/FGH	28.12 ± 0.27^c/δ/EF	14.31 ± 1.66^b/δ/D	0.63 ± 0.54^a/γ/A
	4	38.26 ± 1.56^d/ε/EF	36.95 ± 1.84^d/δ/DE	27.78 ± 0.79^c/δ/EF	9.81 ± 0.52^b/ε/C	0.00^a/γ/A
6	0	63.52 ± 0.99^a/α/O	63.52 ± 0.99^a/α/M	63.52 ± 0.99^a/α/J	63.52 ± 0.99^a/α/K	63.52 ± 0.99^a/α/E
	1	50.55 ± 1.57^e/β/KL	47.35 ± 0.49^d/β/JK	38.92 ± 0.51^c/β/GH	28.73 ± 1.85^b/β/I	5.61 ± 0.66^a/β/CD
	2	47.50 ± 0.62^e/γ/J	45.16 ± 0.96^d/γ/IJ	36.51 ± 0.61^c/γ/G	23.53 ± 1.49^b/γ/FG	1.86 ± 0.60^a/γ/A
	3	44.14 ± 0.69^e/δ/I	40.85 ± 0.97^d/δ/G	30.43 ± 0.58^c/δ/F	20.23 ± 1.07^b/δ/E	0.68 ± 0.60^a/γ/A
	4	40.59 ± 1.94^d/ε/FGH	40.62 ± 0.78^d/δ/FGH	28.42 ± 0.53^c/δ/EF	14.48 ± 1.79^b/ε/D	0.00^a/γ/A
7	0	63.52 ± 0.99^a/α/O	63.52 ± 0.99^a/α/M	63.52 ± 0.99^a/α/J	63.52 ± 0.99^a/α/K	63.52 ± 0.99^a/α/E
	1	53.53 ± 0.86^d/β/MN	51.78 ± 1.45^d/β/L	41.95 ± 1.01^c/β/I	33.75 ± 0.78^b/β/J	8.15 ± 0.61^a/β/D
	2	50.51 ± 1.61^e/γ/KL	47.68 ± 0.52^d/γ/JK	38.92 ± 0.51^c/γ/GH	28.73 ± 1.85^b/γ/I	5.61 ± 0.66^a/γ/CD
	3	47.70 ± 1.05^e/δ/J	45.46 ± 0.44^d/δ/IJK	36.51 ± 0.61^c/δ/G	23.86 ± 1.22^b/δ/FGH	2.86 ± 0.59^a/δ/AB
	4	44.19 ± 0.64^e/ε/I	40.65 ± 0.63^d/ε/GH	30.43 ± 0.58^c/ε/F	21.56 ± 0.65^b/ε/EF	0.75 ± 0.67^a/ε/A
8	0	63.52 ± 0.99^a/α/O	63.52 ± 0.99^a/α/M	63.52 ± 0.99^a/α/J	63.52 ± 0.99^a/α/K	63.52 ± 0.99^a/α/E
	1	54.87 ± 1.40^e/β/N	52.44 ± 2.01^d/β/L	41.62 ± 0.50^c/β/HI	34.61 ± 0.76^b/β/J	9.15 ± 0.49^a/β/D
	2	51.18 ± 1.08^e/γ/LM	48.37 ± 0.59^d/γ/K	39.58 ± 0.55^c/β/GHI	32.06 ± 3.22^b/γ/J	6.94 ± 0.61^a/γ/CD
	3	48.13 ± 0.99^d/δ/JK	45.93 ± 0.94^d/δ/JK	36.84 ± 0.57^c/γ/G	26.53 ± 0.94^b/δ/HI	4.86 ± 0.55^a/γ/BC
	4	45.86 ± 0.97^e/ε/J	42.65 ± 0.63^d/ε/HI	31.78 ± 0.55^c/δ/F	24.52 ± 0.42^b/δ/GH	1.09 ± 0.17^a/δ/A

Open in a new tab

Values are mean ± SD (n = 3); Values within the same row between the temperatures, which do not share similar letters in the superscript are significantly different (p ≤ 0.05) as determined by three-way ANOVA and Tukey’s multiple comparison test. Significantly different (p ≤ 0.05) values within the same column are indicated by dissimilar capitalized letters and the same for every pH are indicated by dissimilar Greek letters in the superscript

Conclusion

To summarize, lutein is a dietary carotenoid which when consumed orally can provide definite health benefits to humans. Since lutein is highly photolabile and thermolabile, processing conditions employed prior to consumption hinder its bioactivity. This study has provided clarity on the extent of degradation caused by such processing conditions with respect to temperature, pH and duration of the operation. Although lutein is highly unstable, processing at low temperatures for short duration maintaining neutral pH can significantly reduce its degradation. Further, this study can pave way for researchers and nutraceutical industries that are trying to minimize lutein loss during pre-processing of its sources.

Supplementary Information

Below is the link to the electronic supplementary material.

Supplementary file1 (DOCX 119 kb)^{(120KB, docx)}

Acknowledgements

The authors express their sincere gratitude to Prof. Dr. Praveenkumar Shetty, Director (R&D), Nitte (DU) and Prof. Dr. Anirban Chakraborty, Director (NUCSER), Nitte (DU) for providing research facilities. The authors are grateful to Prof. Dr. Indrani Karunasagar, Director (DST-NUTEC), Nitte (DU) and Prof. Dr. Iddya Karunasagar, Advisor (Research and Patent), Nitte (DU) for their constant support and guidance. The authors acknowledge the Indian Council of Medical Research, New Delhi, India for funding this study.

Author contributions

Ishani Bhat: Writing-original draft, Visualization, Formal analysis, Validation; Nimmy Mol Jose: Formal analysis; Bangera Sheshappa Mamatha: Supervision, Project administration, Funding acquisition, Writing-review and editing.

Funding

This study was funded by the Indian Council of Medical Research, New Delhi, India.

Availability of data and material

All the relevant data available is mentioned in the manuscript and no other supplementary data is provided.

Declarations

Conflict of interest

None.

Consent for publication

Not applicable since the data was curated by the authors.

Footnotes

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Contributor Information

Ishani Bhat, Email: ishanibhat@gmail.com.

Nimmy Mol Jose, Email: nimmy9605@gmail.com.

Bangera Sheshappa Mamatha, Email: mamatha.bs@nitte.edu.in.

References

Bhat I, Mamatha BS. Genetic factors involved in modulating lutein bioavailability. Nutr Res. 2021;91:36–43. doi: 10.1016/j.nutres.2021.04.007. [DOI] [PubMed] [Google Scholar]
Bhat I, Yathisha UG, Karunasagar I, Mamatha BS. Nutraceutical approach to enhance lutein bioavailability via nanodelivery systems. Nutr Rev. 2020;78(9):709–724. doi: 10.1093/nutrit/nuz096. [DOI] [PubMed] [Google Scholar]
Bhat I, Baskaran V, Mamatha BS. Influence of fatty acids in edible oils on lutein micellization and permeation in a simulated digestion model. Food Biosci. 2021 doi: 10.1016/j.fbio.2021.101423. [DOI] [Google Scholar]
Bhat I, Iyer S, Fernandes V, Divyashree M, Mamatha BS (2021b) Challenges in oral bioavailability of lutein. In: Albert RM. What to know about carotenoids? New York: Nova Publishers; p27–66.
Boon CS, McClements DJ, Weiss J, Decker EA. Factors influencing the chemical stability of carotenoids in foods. Crit Rev Food Sci Nutr. 2010;50(6):515–532. doi: 10.1080/10408390802565889. [DOI] [PubMed] [Google Scholar]
Castenmiller JJ, West CE. Bioavailability and bioconversion of carotenoids. Annu Rev Nutr. 1998;18(1):19–38. doi: 10.1146/annurev.nutr.18.1.19. [DOI] [PubMed] [Google Scholar]
Cheng CJ, Ferruzzi M, Jones OG. Fate of lutein-containing zein nanoparticles following simulated gastric and intestinal digestion. Food Hydrocoll. 2019;87:229–236. doi: 10.1016/J.FOODHYD.2018.08.013. [DOI] [Google Scholar]
Chung RW, Leanderson P, Gustafsson N, Jonasson L. Liberation of lutein from spinach: effects of heating time, microwave-reheating and liquefaction. Food Chem. 2019;277:573–578. doi: 10.1016/J.FOODCHEM.2018.11.023. [DOI] [PubMed] [Google Scholar]
Dall'Osto L, Cazzaniga S, Bressan M, Paleček D, Židek K, Niyogi KK, Graham RF, Donatas Z, Bassi R. Two mechanisms for dissipation of excess light in monomeric and trimeric light-harvesting complexes. Nature Plants. 2017;3(5):1–9. doi: 10.1038/nplants.2017.33. [DOI] [PubMed] [Google Scholar]
Eriksen JN, Luu AY, Dragsted LO, Arrigoni E. In vitro liberation of carotenoids from spinach and Asia salads after different domestic kitchen procedures. Food Chem. 2016;203:23–27. doi: 10.1016/j.foodchem.2016.02.033. [DOI] [PubMed] [Google Scholar]
Fatani AJ, Al-Rejaie SS, Abuohashish HM, Al-Assaf A, Parmar MY, Ahmed MM. Lutein dietary supplementation attenuates streptozotocin-induced testicular damage and oxidative stress in diabetic rats. BMC Complement Altern Med. 2015;15(1):1–10. doi: 10.1186/s12906-015-0693-5. [DOI] [PMC free article] [PubMed] [Google Scholar]
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Gumus CE, Davidov-Pardo G, McClements DJ. Lutein-enriched emulsion-based delivery systems: impact of Maillard conjugation on physicochemical stability and gastrointestinal fate. Food Hydrocolloids. 2016;60:38–49. doi: 10.1016/j.foodhyd.2016.03.021. [DOI] [Google Scholar]
Gutiérrez-Uribe JA, Rojas-García C, García-Lara S, Serna-Saldivar SO. Effects of lime-cooking on carotenoids present in masa and tortillas produced from different types of maize. Cereal Chem. 2014;91(5):508–512. doi: 10.1094/cchem-07-13-0145-r. [DOI] [Google Scholar]
Kamoshita M, Toda E, Osada H, Narimatsu T, Kobayashi S, Tsubota K, Ozawa Y. Lutein acts via multiple antioxidant pathways in the photo-stressed retina. Sci Rep. 2016;6(1):1–10. doi: 10.1038/srep30226. [DOI] [PMC free article] [PubMed] [Google Scholar]
Komuro M, Shimizu N, Onuma R, Otoki Y, Ito J, Kato S, Higuchi O, Nakagawa K. Analysis of lutein in mugwort (Artemisia Princeps Pamp.) paste and evaluation of manufacturing processes. J Oleo Sci. 2017;66(11):1257–1262. doi: 10.5650/jos.ess17117. [DOI] [PubMed] [Google Scholar]
Mamatha BS, Arunkumar R, Baskaran V. Effect of processing on major carotenoid levels in corn (Zea mays) and selected vegetables: bioavailability of lutein and zeaxanthin from processed corn in mice. Food Bioprocess Technol. 2012;5(4):1355–1363. doi: 10.1007/s11947-010-0403-8. [DOI] [Google Scholar]
Mora-Gutierrez A, Attaie R, de González MN, Jung Y, Woldesenbet S, Marquez SA. Complexes of lutein with bovine and caprine caseins and their impact on lutein chemical stability in emulsion systems: effect of arabinogalactan. J Dairy Sci. 2018;101(1):18–27. doi: 10.3168/jds.2017-13105. [DOI] [PubMed] [Google Scholar]
Murillo AG, Aguilar D, Norris GH, DiMarco DM, Missimer A, Hu S, Smyth JA, Gannon S, Blesso CN, Luo Y, Fernandez ML. Compared with powdered lutein, a lutein nanoemulsion increases plasma and liver lutein, protects against hepatic steatosis, and affects lipoprotein metabolism in guinea pigs. J Nutr. 2016;146(10):1961–1969. doi: 10.3945/jn.116.235374. [DOI] [PubMed] [Google Scholar]
Nolan JM, Loskutova E, Howard AN, Moran R, Mulcahy R, Stack J, Bolger M, Beatty S. Macular pigment, visual function, and macular disease among subjects with Alzheimer's disease: an exploratory study. J Alzheimer's Dis. 2014;42(4):1191–1202. doi: 10.3233/jad-140507. [DOI] [PubMed] [Google Scholar]
Qiu X, Gao DH, Xiang X, Xiong YF, Zhu TS, Liu LG, Sun XF, Hao LP. Ameliorative effects of lutein on non-alcoholic fatty liver disease in rats. World J Gastroenterol. 2015;21(26):8061–8072. doi: 10.3748/wjg.v21.i26.8061. [DOI] [PMC free article] [PubMed] [Google Scholar]
Rai AK, Sanjukta S, Chourasia R, Bhat I, Bhardwaj PK, Sahoo D. Production of bioactive hydrolysate using protease, β-glucosidase and α-amylase of Bacillus spp. isolated from kinema. Bioresour Technol. 2017;235:358–365. doi: 10.1016/j.biortech.2017.03.139. [DOI] [PubMed] [Google Scholar]
Ranganathan A, Sheshappa MB, Baskaran V. Quality characteristics and lutein bioavailability from maize and vegetable-based health food. J Diet Suppl. 2014;11(2):131–144. doi: 10.3109/19390211.2013.859208. [DOI] [PubMed] [Google Scholar]
Renzi-Hammond LM, Bovier ER, Fletcher LM, Miller LS, Mewborn CM, Lindbergh CA, Baxter JH, Hammond BR. Effects of a lutein and zeaxanthin intervention on cognitive function: a randomized, double-masked, placebo-controlled trial of younger healthy adults. Nutrients. 2017;9(11):1246–1259. doi: 10.3390/nu9111246. [DOI] [PMC free article] [PubMed] [Google Scholar]
Sánchez C, Baranda AB, de Marañón IM. The effect of high pressure and high temperature processing on carotenoids and chlorophylls content in some vegetables. Food Chem. 2014;163:37–45. doi: 10.1016/j.foodchem.2014.04.041. [DOI] [PubMed] [Google Scholar]
Shen R, Yang S, Zhao G, Shen Q, Diao X. Identification of carotenoids in foxtail millet (Setaria italica) and the effects of cooking methods on carotenoid content. J Cereal Sci. 2015;61:86–93. doi: 10.1016/j.jcs.2014.10.009. [DOI] [Google Scholar]
Torskangerpoll K, Andersen ØM. Colour stability of anthocyanins in aqueous solutions at various pH values. Food Chem. 2005;89(3):427–440. doi: 10.1016/j.foodchem.2004.03.002. [DOI] [Google Scholar]
Yang C, Fischer M, Kirby C, Liu R, Zhu H, Zhang H, Chen Y, Sun Y, Zhang L, Tsao R. Bioaccessibility, cellular uptake and transport of luteins and assessment of their antioxidant activities. Food Chem. 2018;249:66–76. doi: 10.1016/j.foodchem.2017.12.055. [DOI] [PubMed] [Google Scholar]
Yi J, Fan Y, Yokoyama W, Zhang Y, Zhao L. Characterization of milk proteins–lutein complexes and the impact on lutein chemical stability. Food Chem. 2016;200:91–97. doi: 10.1016/j.foodchem.2016.01.035. [DOI] [PubMed] [Google Scholar]

Associated Data

This section collects any data citations, data availability statements, or supplementary materials included in this article.

Supplementary Materials

Supplementary file1 (DOCX 119 kb)^{(120KB, docx)}

Data Availability Statement

All the relevant data available is mentioned in the manuscript and no other supplementary data is provided.

[CR1] Bhat I, Mamatha BS. Genetic factors involved in modulating lutein bioavailability. Nutr Res. 2021;91:36–43. doi: 10.1016/j.nutres.2021.04.007. [DOI] [PubMed] [Google Scholar]

[CR2] Bhat I, Yathisha UG, Karunasagar I, Mamatha BS. Nutraceutical approach to enhance lutein bioavailability via nanodelivery systems. Nutr Rev. 2020;78(9):709–724. doi: 10.1093/nutrit/nuz096. [DOI] [PubMed] [Google Scholar]

[CR3] Bhat I, Baskaran V, Mamatha BS. Influence of fatty acids in edible oils on lutein micellization and permeation in a simulated digestion model. Food Biosci. 2021 doi: 10.1016/j.fbio.2021.101423. [DOI] [Google Scholar]

[CR4] Bhat I, Iyer S, Fernandes V, Divyashree M, Mamatha BS (2021b) Challenges in oral bioavailability of lutein. In: Albert RM. What to know about carotenoids? New York: Nova Publishers; p27–66.

[CR5] Boon CS, McClements DJ, Weiss J, Decker EA. Factors influencing the chemical stability of carotenoids in foods. Crit Rev Food Sci Nutr. 2010;50(6):515–532. doi: 10.1080/10408390802565889. [DOI] [PubMed] [Google Scholar]

[CR6] Castenmiller JJ, West CE. Bioavailability and bioconversion of carotenoids. Annu Rev Nutr. 1998;18(1):19–38. doi: 10.1146/annurev.nutr.18.1.19. [DOI] [PubMed] [Google Scholar]

[CR7] Cheng CJ, Ferruzzi M, Jones OG. Fate of lutein-containing zein nanoparticles following simulated gastric and intestinal digestion. Food Hydrocoll. 2019;87:229–236. doi: 10.1016/J.FOODHYD.2018.08.013. [DOI] [Google Scholar]

[CR8] Chung RW, Leanderson P, Gustafsson N, Jonasson L. Liberation of lutein from spinach: effects of heating time, microwave-reheating and liquefaction. Food Chem. 2019;277:573–578. doi: 10.1016/J.FOODCHEM.2018.11.023. [DOI] [PubMed] [Google Scholar]

[CR9] Dall'Osto L, Cazzaniga S, Bressan M, Paleček D, Židek K, Niyogi KK, Graham RF, Donatas Z, Bassi R. Two mechanisms for dissipation of excess light in monomeric and trimeric light-harvesting complexes. Nature Plants. 2017;3(5):1–9. doi: 10.1038/nplants.2017.33. [DOI] [PubMed] [Google Scholar]

[CR10] Eriksen JN, Luu AY, Dragsted LO, Arrigoni E. In vitro liberation of carotenoids from spinach and Asia salads after different domestic kitchen procedures. Food Chem. 2016;203:23–27. doi: 10.1016/j.foodchem.2016.02.033. [DOI] [PubMed] [Google Scholar]

[CR11] Fatani AJ, Al-Rejaie SS, Abuohashish HM, Al-Assaf A, Parmar MY, Ahmed MM. Lutein dietary supplementation attenuates streptozotocin-induced testicular damage and oxidative stress in diabetic rats. BMC Complement Altern Med. 2015;15(1):1–10. doi: 10.1186/s12906-015-0693-5. [DOI] [PMC free article] [PubMed] [Google Scholar]

[CR12] Gouveia L, Empis J. Relative stabilities of microalgal carotenoids in microalgal extracts, biomass and fish feed: effect of storage conditions. Innov Food Sci Emerg Technol. 2003;4(2):227–233. doi: 10.1016/S1466-8564(03)00002-x. [DOI] [Google Scholar]

[CR13] Gumus CE, Davidov-Pardo G, McClements DJ. Lutein-enriched emulsion-based delivery systems: impact of Maillard conjugation on physicochemical stability and gastrointestinal fate. Food Hydrocolloids. 2016;60:38–49. doi: 10.1016/j.foodhyd.2016.03.021. [DOI] [Google Scholar]

[CR14] Gutiérrez-Uribe JA, Rojas-García C, García-Lara S, Serna-Saldivar SO. Effects of lime-cooking on carotenoids present in masa and tortillas produced from different types of maize. Cereal Chem. 2014;91(5):508–512. doi: 10.1094/cchem-07-13-0145-r. [DOI] [Google Scholar]

[CR15] Kamoshita M, Toda E, Osada H, Narimatsu T, Kobayashi S, Tsubota K, Ozawa Y. Lutein acts via multiple antioxidant pathways in the photo-stressed retina. Sci Rep. 2016;6(1):1–10. doi: 10.1038/srep30226. [DOI] [PMC free article] [PubMed] [Google Scholar]

[CR16] Komuro M, Shimizu N, Onuma R, Otoki Y, Ito J, Kato S, Higuchi O, Nakagawa K. Analysis of lutein in mugwort (Artemisia Princeps Pamp.) paste and evaluation of manufacturing processes. J Oleo Sci. 2017;66(11):1257–1262. doi: 10.5650/jos.ess17117. [DOI] [PubMed] [Google Scholar]

[CR17] Mamatha BS, Arunkumar R, Baskaran V. Effect of processing on major carotenoid levels in corn (Zea mays) and selected vegetables: bioavailability of lutein and zeaxanthin from processed corn in mice. Food Bioprocess Technol. 2012;5(4):1355–1363. doi: 10.1007/s11947-010-0403-8. [DOI] [Google Scholar]

[CR18] Mora-Gutierrez A, Attaie R, de González MN, Jung Y, Woldesenbet S, Marquez SA. Complexes of lutein with bovine and caprine caseins and their impact on lutein chemical stability in emulsion systems: effect of arabinogalactan. J Dairy Sci. 2018;101(1):18–27. doi: 10.3168/jds.2017-13105. [DOI] [PubMed] [Google Scholar]

[CR19] Murillo AG, Aguilar D, Norris GH, DiMarco DM, Missimer A, Hu S, Smyth JA, Gannon S, Blesso CN, Luo Y, Fernandez ML. Compared with powdered lutein, a lutein nanoemulsion increases plasma and liver lutein, protects against hepatic steatosis, and affects lipoprotein metabolism in guinea pigs. J Nutr. 2016;146(10):1961–1969. doi: 10.3945/jn.116.235374. [DOI] [PubMed] [Google Scholar]

[CR20] Nolan JM, Loskutova E, Howard AN, Moran R, Mulcahy R, Stack J, Bolger M, Beatty S. Macular pigment, visual function, and macular disease among subjects with Alzheimer's disease: an exploratory study. J Alzheimer's Dis. 2014;42(4):1191–1202. doi: 10.3233/jad-140507. [DOI] [PubMed] [Google Scholar]

[CR21] Qiu X, Gao DH, Xiang X, Xiong YF, Zhu TS, Liu LG, Sun XF, Hao LP. Ameliorative effects of lutein on non-alcoholic fatty liver disease in rats. World J Gastroenterol. 2015;21(26):8061–8072. doi: 10.3748/wjg.v21.i26.8061. [DOI] [PMC free article] [PubMed] [Google Scholar]

[CR22] Rai AK, Sanjukta S, Chourasia R, Bhat I, Bhardwaj PK, Sahoo D. Production of bioactive hydrolysate using protease, β-glucosidase and α-amylase of Bacillus spp. isolated from kinema. Bioresour Technol. 2017;235:358–365. doi: 10.1016/j.biortech.2017.03.139. [DOI] [PubMed] [Google Scholar]

[CR23] Ranganathan A, Sheshappa MB, Baskaran V. Quality characteristics and lutein bioavailability from maize and vegetable-based health food. J Diet Suppl. 2014;11(2):131–144. doi: 10.3109/19390211.2013.859208. [DOI] [PubMed] [Google Scholar]

[CR24] Renzi-Hammond LM, Bovier ER, Fletcher LM, Miller LS, Mewborn CM, Lindbergh CA, Baxter JH, Hammond BR. Effects of a lutein and zeaxanthin intervention on cognitive function: a randomized, double-masked, placebo-controlled trial of younger healthy adults. Nutrients. 2017;9(11):1246–1259. doi: 10.3390/nu9111246. [DOI] [PMC free article] [PubMed] [Google Scholar]

[CR25] Sánchez C, Baranda AB, de Marañón IM. The effect of high pressure and high temperature processing on carotenoids and chlorophylls content in some vegetables. Food Chem. 2014;163:37–45. doi: 10.1016/j.foodchem.2014.04.041. [DOI] [PubMed] [Google Scholar]

[CR26] Shen R, Yang S, Zhao G, Shen Q, Diao X. Identification of carotenoids in foxtail millet (Setaria italica) and the effects of cooking methods on carotenoid content. J Cereal Sci. 2015;61:86–93. doi: 10.1016/j.jcs.2014.10.009. [DOI] [Google Scholar]

[CR28] Torskangerpoll K, Andersen ØM. Colour stability of anthocyanins in aqueous solutions at various pH values. Food Chem. 2005;89(3):427–440. doi: 10.1016/j.foodchem.2004.03.002. [DOI] [Google Scholar]

[CR29] Yang C, Fischer M, Kirby C, Liu R, Zhu H, Zhang H, Chen Y, Sun Y, Zhang L, Tsao R. Bioaccessibility, cellular uptake and transport of luteins and assessment of their antioxidant activities. Food Chem. 2018;249:66–76. doi: 10.1016/j.foodchem.2017.12.055. [DOI] [PubMed] [Google Scholar]

[CR30] Yi J, Fan Y, Yokoyama W, Zhang Y, Zhao L. Characterization of milk proteins–lutein complexes and the impact on lutein chemical stability. Food Chem. 2016;200:91–97. doi: 10.1016/j.foodchem.2016.01.035. [DOI] [PubMed] [Google Scholar]

PERMALINK

Oxidative stability of lutein on exposure to varied extrinsic factors

Ishani Bhat

Nimmy Mol Jose

Bangera Sheshappa Mamatha

Abstract

Supplementary Information

Introduction

Materials and methods

Chemicals

Lutein extraction and purification

Experimental design

Fig. 1.

Lutein extraction after exposure

HPLC analysis

Antioxidant activity

Statistical analysis

Results and discussion

Purification of lutein

Fig. 2.

Effect of pH on lutein

Fig. 3.

Table 1.

Effect of temperature on lutein

Duration of exposure

Functional stability of lutein

Table 2.

Conclusion

Supplementary Information

Acknowledgements

Author contributions

Funding

Availability of data and material

Declarations

Conflict of interest

Consent for publication

Footnotes

Contributor Information

References

Associated Data

Supplementary Materials

Data Availability Statement

ACTIONS

PERMALINK

RESOURCES

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