XII Congreso CYTAL - AATA

Facultad de Ciencias de la Alimentación, UNER,

Entre Ríos, Argentina, 7-9 de octubre 2009

EFFECTS OF LEAF AGE AND TEMPERATURE ON SEVERAL QUALITY

INDICES OF BUTTERHEAD LETTUCE DURING FIRST HOURS AFTER
HARVEST.

Agüero M.V.1,2,*; Ponce, A.G.1,2; Bevilacqua A2,3; and Roura SI1,2

1
Grupo de Investigación en Ingeniería en Alimentos. Facultad de Ingeniería. Universidad Nacional de Mar del
Plata. Juan B. Justo 4302. Zip code: 7600. Mar del Plata. Argentina, mvaguero@fi.mdp.edu.ar. 2CONICET.
3
Departamento de Ingeniería Química. Facultad de Ingeniería Universidad Nacional de La Plata.

Abstract: Whole lettuce plants were used to evaluate the effect of leaf age (and
exposure level) on ascorbic acid (A), chlorophyll (C), microbial quality (M), colour
and overall visual quality of fresh butterlettuce exposed at three isothermal
environmental conditions: 0-2, 10-12 and 20-22ºC during first hours after harvest.
Temperature, leaf age and time significantly affect the quality parameters under
study. Detriment of lettuce quality was detected in the first few hours after harvest.
In general terms, decreases in quality indices were higher at higher temperature and
time. Outer leaves (older leaves) resulted the most affected tissue by exposure
conditions, while inner leaves (younger) were the least affected.
Keywords: lettuce, leaf age, temperature, quality indices.

INTRODUCTION The objective of the present research was to

Fresh vegetables are highly perishable products and
its shelf life is mainly affected by handling
procedures, temperature, and relative humidity
(Kader 2002). Rapid management from farm to
table, and at optimal conditions, is a desirable
feature because it minimizes economical and
quality losses during postharvest (Jones et al.
1998). Effects of temperature over quality
detriment of crops have been extensively studied
and they are well known. However, few researches
have been developed to investigate the first few
hours after harvest together with leaf age and
exposure level (Moreira et al. 2006; Jedermamm et
al. 2007)
Lettuce is one of the most popular leafy vegetables
in the world. In Argentine farms, lettuce bins are
usually exposed to inadequate and uncontrolled
field conditions (usually high temperature) while it
is waiting to be transported from the field to
distribution centers. So the knowledge of the events
occurring within the plant when temperature is
uncontrolled during first hours after harvest is of
fundamental importance to improve and optimize
lettuce management.
The lettuce head is an assemblage of heterogenic
morphological leaves (Wien, 1997). Its formation
results from the accumulation of young leaves
under the layers of leaves covering the growing
point (Johnson, 1983). Several studies have been
demonstrated that these differences are reflected in
the composition of leaves and its metabolic activity
(Siomos et al. 2002; Del Nobile et al. 2006; Agüero
et al. 2008). In this way, the response of lettuce
tissue to temperature could be affected be the leaf
age.
describe the response of different lettuce leaves
(outer, mid and inner) to the exposure at three
isothermal conditions (0-2, 10-12 and 20-22ºC)
during the first hours after harvest. Evaluated
responses were several quality indicators: a) total
chlorophyll content and b) colour changes as
greenness indexes, c) total microbial counts and as
microbiological descriptor, and d) ascorbic acid
retention as nutritional index.
MATERIAL AND METHODS
Plant Material and Sample Preparation
Heads of greenhouse Butter lettuce (Lactuca sativa
var. Lores) were grown in Sierra de los Padres, Mar
del Plata, Argentina; and were harvested at optimal
maturity. Once harvested, lettuce heads were
immediately transported to the laboratory, were six
whole plants were analyzed to obtain the initial
value for each quality parameter.
Plants were exposed at three different isothermal
conditions (all at optimal relative humidity
recommended for lettuce: 97-99%): 0-2ºC (optimal
temperature), 10-12ºC and 20-22 ºC. Temperatures
of 10-12ºC and 20-22ºC were chosen to simulate
abusive refrigerated and room warm temperatures,
respectively. Sampling was carried out at 0, 3, 6
and 24 hours after harvest.
All parameters were measured in three different
zones of the lettuce head called external (outer and
older leaves), middle (mid leaves) and internal zone
(inner and younger leaves) (Agüero et al. 2008).
Three independent experimental runs were done.

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XII Congreso CYTAL - AATA
Facultad de Ciencias de la Alimentación, UNER,
Entre Ríos, Argentina, 7-9 de octubre 2009
Total Chlorophyll Content
To determine Total Chlorophyll Content (TC), all
leaves in each zone were homogenized with a
commercial blender (Multiquick, MR 5550 CA
Braun, Espanola S.A., Barcelona, Spain) and two
samples (1 g each) were taken from each
homogenate. Each sample was then homogenized
with 19 ml of a cold solution 18:1 propanone:
ammonium hydroxide (0.1N). This homogenate
was filtered through sintered glass and water was
removed from the filtrate with anhydrous sodium
sulfate. Absorbance of the filtrate at 660.0 and
642.5 nm was measured with a UV 1601 PC UV-
visible spectrophotometer (Shimadzu Corporation,
Japan). Total Chlorophyll was calculated applying
the formula TC = 7.12A660 + 16.8 A642.5; in which
TC is the total chlorophyll concentration (mg L-1)
and A660 and A642.5 are the absorbance at the
corresponding wavelengths. TC is reported as mg
of chlorophyll / 100 g fresh weight.
Total Microbial Counts
The enumeration of total microorganisms was
performed. Ten grams of leaves were macerated in
a buffer solution (PO4K3, pH=7.2). Microbial
counts were carried out using Plate Count Agar
(PCA) incubated at 32-35 ºC for 48-72 h (ICMSF
1983). The culture media was from Britania
(Buenos Aires, Argentina). Studies were performed
by duplicate. Microbiological counts were
expressed as log CFU / g of fresh weight.
Reduced Ascorbic Acid content
To determine reduced ascorbic acid content, ground
lettuce leaves (20 g) were extracted with 100 mL of
metaphosphoric acid solution (60 g.Kg-1) for 3 min
using a commercial blender (Multiquick, MR 5550
CA Braun, Espanola S.A., Barcelona, Spain) with
an homogenizer speed of 3500 to 7000 rpm. The
homogenate was made up to 250 mL with 30 g.Kg-
1 metaphosphoric acid and filtered through
Whatman n° 42 filter paper. Temperature during
ascorbic acid extraction was maintained at 0°C.
Three aliquots (5 mL each) of the filtrate were
titrated with 2,6- dichloroindophenol. Ascorbic acid
contents were reported as mg / 100 g of fresh
weight.
Colour
Colour determination was carried out using a
Minolta colorimeter CR 300 Series (Osaka, Japan)
with an 8 mm diameter measuring area. The colour
was measured by L, a* and b* chromaticity co-
ordinates of the CIELab* scale. The instrument was
calibrated with a standard white plate (L = 93.97,
a* = -21.85 and b* = 1.21). Colour was measured
in all leaves integrating each lettuce zone. Ten
different points were at least measured in each leaf.
Mean values for L, a* and b* parameters were
calculated for each leaf, and then for each zone.
Sensorial evaluation
Immediately after lettuces were removed from
storage conditions, a panel composed by 9 trained
judges proceeded to the assessment. The coded (3
digit) samples were presented one at the time in
random order to the judges. The judges were asked
to evaluate overall visual quality of lettuce heads
taking into account the following characteristics:
color (shade and uniformity), texture, browning and
presence/absence of defects. A 9-point scale was
used, where 9= excellent, 5= acceptable and 1=
poor (Kader 2002).
Statistical Analysis
Results reported, are LSMEAN values (least square
mean, means estimators by the method of least
squares) together with their standard deviations
(Khuel 2001). Data were analyzed using SAS,
software version 8.0 (SAS Inc. 1999). PROC GLM
(General linear model procedure) was used for the
analysis of variance (ANOVA). For all parameters,
except sensorial quality, the factors employed as
sources of variation were: TIME (time after
harvest), PLANT WITHIN TIME, ZONE (zone of
the plant), TEMPERATURE and interactions:
TIME-ZONE; TIME-TEMPERATURE and TIME-
ZONE-TEMPERATURE. Differences between
zones, temperatures and time were determined by
the Tukey-Kramer multiple comparison test (p<
0.05). For sensorial quality data, the factor ZONE
was not taken into account in order that overall
visual quality was evaluated in the whole lettuce
plant.
RESULTS AND DISCUSSION
Total Chlorophyll Content
Initial chlorophyll content (TC) in harvested lettuce
was significantly affected by leaf age (Table 1),
being the content of the external zone 5 times
higher than that of the internal one. The higher
exposure of outer leaves to sun light respect inner
leaves could be responsible for the differences in
chlorophyll concentrations between zones.
Table 1. Quality indices at harvest.
Quality Lettuce zone
parameter External Middle Internal
Chlorophyll 51,74 ± 1,93a 22,13 ± 2,11b 10,60 ± 1,76c
L* 59,113 ± 1,95b 65,71 ± 3,38b 76,06 ± 2,00a
a* -19,73 ± 0,83 a
-19,25 ± 1,28 a
-16,30 ± 1,25b
b* 34,64 ± 0,88c 37,26 ± 0,85b 40,50 ± 0,78a
Microbial
5,95 ± 0,10a 5,83 ± 0,11a 5,64 ± 0,15a
count
Ascorbic acid 9,55 ± 0,58b 11,35 ± 0,68ª 9,52 ± 0,88b
Means with the same superscripts were not significantly
different (P < 0.05).
The exposure of almost all vegetables to inadequate
temperatures brings about certain degradation on
chlorophyll pigments (King et al. 2001; Yongguang
et al. 2007; Zhang at el. 2008). ANOVA applied to
chlorophyll data showed a significant interaction
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XII Congreso CYTAL - AATA
Facultad de Ciencias de la Alimentación, UNER,
Entre Ríos, Argentina, 7-9 de octubre 2009

between ZONE and TIME factors. This fact implies
that each zone have a particular behavior during
postharvest. In this way, while the external zone
exhibited chlorophyll pigments degradation
throughout 24 hours at any assayed temperature, the
middle and internal zones showed no chlorophyll
content changes during such period. Fig. 1 depicts
the evolution of TC in external zone during 24
hours after harvest.
60
(mg / 100 g fresh weight)
in lettuce exposed to different temperature
conditions. The significant differences detected
between zones at harvest were maintained as time
advanced at the three evaluated temperatures; i.e. at
each sampling time and at the three assayed
temperatures, outer and mid leaves resulted more
green (lower a* values) than inner ones. Samples
exposed to the highest temperature registered the
lowest absolute value of a* parameter during the
sampling time in the three lettuce zones. Significant
decreases in the absolute value of a* were observed

50
Chlorophyll content

40
during 24 hours in the three zones and the three
analyzed temperatures and the highest decrease was
30
observed in internal zone at 20-22ºC.
20
10 Table 2 – a* value in external (E), middle (M) and
0 internal (I) zones of lettuce heads during 24 hours of
exposition to three different isothermal conditions (0-2,
0 5 10 15 20 25
10-12 and 20-22ºC).
Time (hours)
Time (h) Zone a* values
Figure 1. Chlorophyll content evolution in external zone E -19,73 ± 0,83
of lettuce heads during 24 hours of exposure to 0 M -19,25 ± 1,28
I -16,30 ± 1,25
isothermal conditions: (U)20ºC; (×)10ºC; (♦)0ºC. 0-2ºC 10-12ºC 20-22ºC
-19,37 ± -19,35 ± -18,89 ±
E
Differences in chlorophyll degradation between 0,32 0,56 0,24
-19,49 ± -18,85 ± -18,90 ±
zones could be related to the higher exposure of 3 M
1,52 0,56 1,07
outer leaves to environmental factors such as light I
-15,89 ± -13,47 ± -12,88 ±
and oxygen, which could fasten pigment 0,88 3,86 1,52
-19,51 ± -18,13 ± -18,93 ±
deterioration. As a response to harvest stress, when E
1,09 2,37 0,03
water and nutrient supply was cut off, outer leaves 6 M
-18,43 ± -16,84 ± -18,03 ±
0,90 0,21 1,61
(the most mature leaves of lettuce head, and leaves -12,86 ± -12,49 ± -12,43 ±
I
that are also near its physiological senescence) 1,04 0,58 2,41
could trigger different physiological responses. At -19,32 ± -19,07 ± -18,87 ±
E
0,34 0,35 0,06
harvest, senescence process is induced artificially -19,14 ± -17,94 ± -17,44 ±
24 M
as a result of the removal of nutrient supplies (Page 0,16 2,26 0,40
-15,26 ± -12,22 ± -11,06 ±
et al. 2001). As a rapid response, the degradation of I
0,76 1,86 2,04
TC was evident in outer leaves, which started
showing signs of chlorophyll losses. A decrease in the absolute value of a* indicates a
Colour reduction of green colour mainly associated with
chlorophyll degradation (Rico et al. 2008).
Lightness parameter (L*) in lettuce at harvest However, in the present work, decreases in
showed significant differences among zones (Table chlorophyll concentration were not detected in
1). The highest L* value was observed in internal internal zone while changes in a* parameter were
zone, decreasing towards the external one. The detected in this zone. Del Nobile et al. (2006),
exposure of lettuce heads to different temperature studying the effect of film packaging on quality and
conditions during 24 hours did not introduce shelf life of lettuce, found the highest changes of a*
significant changes in L* parameter as a function of parameter in inner leaves and associated this result
time or temperature (data not shown). Other authors to the highest susceptibility of this leaves to
(Han et al. 2004; Martínez-Romero et al. 2008) also browning.
found for lettuce no significant changes in L* Blueness/yellowness parameter (b*) in lettuce at
parameter throughout storage time. harvest resulted positive in all zones indicating the
Redness/greenness parameter (a*) in lettuce at predominance of yellow in this scale. Significant
harvest resulted in a negative value in all zones differences between zones were found in b* values
indicating the predominance of green colour in the at harvest, being higher (more yellow) in inner
product. Results showed significant differences leaves than in mid and outer leaves (Table 1). b*
between a* values in each zone at harvest, being values obtained for lettuce zones during time of
more negative (more green) in external and middle exposure to different temperatures are presented in
zones (without significant differences between Table 3. During the sampling time no changes were
them) than in internal one (Table 1). Green colour registered in b* values as time advanced at any
of inner leaves is less intense and this fact was analyzed temperature and zone. Moreover,
reflected in a* values obtained for each zone. Table significant differences in b* values detected among
2 presents a* values obtained during sampling time lettuce zones at harvest were maintained as time

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XII Congreso CYTAL - AATA
Facultad de Ciencias de la Alimentación, UNER,
Entre Ríos, Argentina, 7-9 de octubre 2009

advanced at the three evaluated temperatures. It was Ascorbic acid content

found that samples exposed to high temperatures
Initial ascorbic acid (AA) content in middle zone
registered lowest values of b* parameter.
resulted significantly higher in middle zone than in
Table 3 – b* value in external (E), middle (M) and external and internal ones. (Table 1). This could be
internal (I) zones of lettuce heads during 24 hours of related to the degree of tissue development. Outer
exposition to three different isothermal conditions (0-2, leaves, being older and more senescent tissue had
10-12 and 20-22ºC). lower AA contents because degradative reactions
Time (h) Zone b* values may have begun in this leaves. Inner leaves, being
E 34,64 ± 0,88 the youngest tissue in the lettuce plant, have lower
0 M 37,26 ± 0,85
I 40,50 ± 0,78 AA content than mid leaves probably because the
0-2ºC 10-12ºC 20-22ºC AA synthesis in young tissue is lower than in fully
E 35,05 ± 34,81 ± 34,03 ± expanded leaves (mid leaves).
0,05 0,22 1,83
M 38,25 ± 38,29 ± 35,73 ± Numerous factors affect AA degradation, mainly
3
0,75 1,24 2,41 temperature, salt and sugar concentrations, pH,
I 42,18 ± 39,18 ± 38,27 ± oxygen, enzymes, among others (Davey et al.
3,49 4,46 0,40
E 36,45 ± 33,77 ± 33,72 ± 2000). At each temperature and at each sampling
0,54 3,35 0,09 time, the three zones presented similar AA values.
M 37,34 ± 34,27 ± 34,42 ±
6
2,53 1,82 4,47 For this reason, the three zones were considered
I 42,31 ± 39,08 ± 36,92 ± together as a pool of data to compare effect of
2,85 5,83 2,95 temperature and time (Fig 3).
E 34,19 ± 34,31 ± 33,69 ±
0,56 0,02 0,52 12

(mg / 100 g fresh weight)

M 36,96 ± 34,21 ± 33,07 ±
24 10
1,93 2,79 1,53
Ascorbic Acid
I 46,09 ± 37,92 ± 33,24 ± 8
0,56 6,32 6,14
6
4
Total microbial counts 2
The largest population in green vegetables is the 0
mesophilic microflora (Watada 1996). Initial 0 5 10 15 20 25
microbial counts for external, middle and internal Time (hours)
zones were not significantly different (Table 1).
This fact could express that microorganisms found Figure 3. LSMEANS for Ascorbic acid content evolution
similar preharvest environmental and nutritional in the three zones together during 24 hours of exposure to
isothermal conditions: (U)20ºC; (×)10ºC; (♦)0ºC.
conditions in each zone. Fig. 2 shows total
increments in microbial counts for each lettuce
zone at each temperature (LOG(Nt/N0)). Microbial The highest AA contents corresponded to lettuces
counts evolution during 24 hours differed taking exposed to 0ºC during the entire sampling period.
into account the zone and the temperature. In the The behavior of AA at 10 and 20ºC did not present
three lettuce zones increments in microbial counts significant differences between them but they were
occurred during the first 24 hours of exposure to lower than values at 0ºC. AA decreases during the
different temperatures, being higher in external 24 h at the three assayed temperatures. When
zone with respect to middle and internal ones and temperature was 10 or 20ºC, losses of about 50%
resulting greater when temperature was 20ºC were detected in the first 6 hours, while 30% of
instead of 10ºC or 0ºC. losses were detected at 0ºC in this time. At the end
of the 24 hours of sampling, losses reached 40% (at
4,0 0ºC) and 50% (at 10 and 20ºC). Losses of AA at
optimal temperature (0-2ºC) could be associated to
LOG (N24/N0)

3,0
External
stress induced by harvest (Davey et al. 2000; Lee et
2,0
Middle
al. 1982).
1,0 Internal Sensorial quality
0,0
Table 4 shows changes in overall visual quality
0 10 20
(OVQ) of lettuce head during 24 hours of the
Temperature(ºC) exposure to different temperatures. Panelists did not
detect significant changes in OVQ of lettuce heads
Figure 2. Microbial counts change (LOG(N24/N0) ) in exposed to optimal temperature. When lettuce
external, middle and internal zone of lettuce heads after heads were exposed to abusive temperatures,
24 hours of exposure to isothermal conditions. panelists detected significant decreases in OVQ at
24 hours of exposure (p= 0.0021 and p< 0.0001,
respectively). Main differences were registered at
24 h in texture quality of lettuce heads exposed to

4
XII Congreso CYTAL - AATA
Facultad de Ciencias de la Alimentación, UNER,
Entre Ríos, Argentina, 7-9 de octubre 2009
10 and 20ºC. Panelists detected moderate losses of
turgidity and texture. Another phenomenon
detected by panelists was the degree of browning
developed in the base of the lettuce due to the cut
made during picking. At 24 h of exposure, lettuces
at 10-12 and 20-22ºC presented cut bases with
moderate and objectionable browning to severe
browning (rusty-brown), respectively. At optimal
exposed temperature, only slight and not
objectionable browning in the cut base was
detected. After 24 h of storage the best quality
attributes were observed in lettuces exposed to
optimal temperature immediately after harvest.
Table 4 – Overall visual quality of lettuce head during the
exposure to three different isothermal conditions (0-2 ºC,
10-12 ºC and 20-22 ºC).
Time (h) Initial OVQ
0 9 ± 0.1
0-2ºC 10-12ºC 20-22ºC
3 8.9 ± 0.1 8.9 ± 0.2 8.9 ± 0.1
6 8.9 ± 0.1 8.8 ± 0.1 8.7 ± 0.3
24 8.5 ± 0.5 8.1 ± 0.3 7.5 ± 0.6
CONCLUSION
Leaf age had a significant effect on the initial
greenness and nutritional indices of butterhead
lettuce. Older leaves (external zone) showed higher
chlorophyll concentration and lower L* and a*
values, than younger leaves characterized by
clearest colour (high L* and a* values and low
chlorophyll content). Ascorbic acid in mid leaves
resulted higher than in outer and inner leaves.
Microbial counts in lettuce at harvest were not
affected by leaf age, showing the three lettuce
zones, similar values of these parameters.
Detriment in butterhead lettuce initial quality
begins in the first hours after harvest and was
affected by both temperature and leaf age.
Important nutritional losses occurred even though
lettuces were exposed to optimal temperature (0-
2ºC), however losses were more important at higher
abusive temperature. Leaf age did not affect the
degradation of ascorbic acid and the three lettuce
zones showed similar degradation pattern only
affected by temperature. Chlorophyll losses were
detected at 3 hours of storage at the three exposure
temperatures and were only evident in outer leaves.
Mid and inner leaves did not show any change in its
chlorophyll contents during 24 h of exposure at
different temperatures. From a bacteriological point
of view, 24 h of exposure to both 10 and 20ºC
dangerously increased the number of microbial
counts diminishing the microbiological quality of
the product. In conclusion, maintaining the correct
storage and transport temperature from the harvest
to the consumer is an important factor in
minimizing quality loss. Despite this, it is often
overlooked. This is sometimes due to commercial
constraints, but it can also be due to a lack of
information. The knowledge of the effect of leaf
age on the evolution of quality indices is of
fundamental importance for producers because they
can take decisions in order of this differential
behavior according to degree of development of
tissue. In this way they could use different lettuce
leaves for different uses as fresh consumption,
minimally processed products, among others.
ACKNOWLEDGEMENTS
This work was supported by Consejo Nacional de
Investigaciones Científicas y Técnicas (CONICET),
Agencia Nacional de Promoción Científica y
Tecnológica (Secyt), and Universidad Nacional de
Mar del Plata (UNMDP).
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