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Guinea Pigs in Balance: Impact of Diet on pH, Microbiota and Intestinal Performance

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03 September 2024

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03 September 2024

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Abstract
The study assessed the impact of different diets on gastrointestinal pH, intestinal microbiota, digestive tract morphometry, and productive performance in guinea pigs. A total of 160 improved genotype guinea pigs were used, distributed into three groups with different diets: alfalfa (T1), alfalfa + concentrate (T2), and concentrate (T3), to which a mixture of probiotics combined with vitamins, minerals was added and amino acids in T2 and T3. Gastrointestinal pH showed significant differences between treatments in the various segments of the digestive tract. The intestinal microbiota varied according to the diet, with Escherichia coli being the predominant bacterium in weaned guinea pigs. Intestinal morphometry was significantly altered with the addition of a reinforced probiotic mixture, improving the length and density of intestinal villi. Productive parameters such as weight gain, feed consumption, and feed conversion were better in guinea pigs fed a mixed diet with 0.5% probiotic mixture. These results indicate that intestinal pH may influence microbial composition, which impacts productive efficiency and immune health, highlighting the importance of balanced nutrition and supplementation to optimize the health and performance of guinea pigs.
Keywords: 
Subject: Biology and Life Sciences  -   Animal Science, Veterinary Science and Zoology

1. Introduction

The relationship between diet and animal health, as well as the interaction between gastrointestinal microbiota and metabolism, has been studied for decades, and its importance continues to be relevant in the field of animal production [1]. In this context, guinea pigs (Cavia porcellus) emerge as an invaluable model due to their herbivorous nature and their widespread use in meat production in many regions of the world [2]. Diet plays a crucial role in performance and significantly influences various physiological and metabolic aspects of animals. However, the relationship between diet and parameters such as gastrointestinal pH, intestinal microbiota composition, intestinal morphometry, and productive performance has not yet been fully elucidated in guinea pigs.
Diet can alter the functional metabolism of the intestinal microbiome [3] and, along with genetic factors and certain additives, influence the predominance of some microorganisms over others [4]. Moreover, the microbiota is associated with body growth, immune development, and nutrition [5,6,7], while intestinal morphometry provides invaluable information on nutrient absorption capacity and gastrointestinal tract health. Similarly, gastrointestinal pH can either promote or hinder digestion and nutrient absorption [8]. For example, in rabbits, exposure to excessive amounts of easily fermentable substrates (proteins and starch) leads to hyperfermentation when incompletely ingested before reaching the cecum, causing changes in cecal pH and inhibiting normal microbiota [9]. In non-herbivorous monogastrics such as chickens, protein-rich diets cause an alkaline pH at the cecum, promoting intestinal health and productive parameters [10].
Despite existing evidence on the influence of diet on these physiological aspects, a deeper understanding is still needed of how different dietary components can modulate gastrointestinal pH, which in turn may affect probiotic mechanisms. This is especially relevant considering the discrepancies in the results reported in various studies using Lactobacillus to improve the productive performance of guinea pigs.
The present study analyzed the impact of different diets on gastrointestinal pH, intestinal microbiota composition, digestive tract morphometry, and guinea pig performance. It is expected that the findings of this research will contribute to the design of more effective nutritional strategies to improve the health and performance of these animals in production systems.

2. Materials and Methods

2.1. Study Area

The trial was conducted in the Azuay province, Cuenca canton, Ecuador, at an average altitude of 2,500 meters above sea level, with an annual average temperature of 14.6ºC and an average precipitation of 900 mm per year [11]. A total of 160 improved genotype guinea pigs were used, weaned at 21 days of age, with an average weight of 351 g for males and 307 g for females. The animals were randomly assigned to three treatments: T1 (Alfalfa - Medicago sativa), T2 (Alfalfa + Concentrate), and T3 (Concentrate), with four subgroups per treatment and 10 animals per subgroup (9 females and 1 male). After three weeks, 2 females were removed from each subgroup for euthanasia, leaving groups of 7 females and 1 male, as recommended by Cruz [12].

2.2. Zootechnical Management of Guinea Pigs

The identification of the animals was carried out by placing a numbered metal tag on the left ear pavilion. The environmental variables within the pen (temperature, humidity, and light), density, and health program were similar for all experimental units. The nutritional program was adjusted according to the nutritional requirements based on the physiological stage of the guinea pigs.

2.3. Procedure

The study was divided into two phases:

2.3.1. First Phase

The influence of diet on the gastrointestinal pH of the guinea pigs was analyzed. A 7-day adaptation period to the diet was implemented. After 21 days, 8 female guinea pigs per treatment (2 per group) were selected for euthanasia using Sodium Pentobarbital (25-40 mg/kg) administered intravenously, following the recommendations for the euthanasia of experimental animals issued by Close et al. [13,14]. Subsequently, the gastrointestinal tract segments (stomach, duodenum, jejunum, ileum, and cecum) were exposed, and the pH of these segments was measured using pH strips.

2.3.2. Second Phase

The study investigated whether the variability in pH recorded with the three diets influenced the mechanism of action of the enhanced probiotic mixture (Probiolyte® WS), incorporated at 0.5% in T2 and 1% in T3, with T1 serving as the control treatment. To identify the gut microbiota of the lactating guinea pigs and those in T2 and T3, samples were first plated on specific culture media using streaking techniques to facilitate the isolation of individual colonies. The isolated colonies were then purified on fresh culture media to ensure pure cultures. Once pure colonies were obtained, MALDI-TOF MS (Matrix-Assisted Laser Desorption Ionization-Time of Flight-Mass Spectrometry) technology was used for identification due to its high precision and speed in microbial species characterization [15].
Additionally, intestinal morphometric parameters (width and length of intestinal villi and Lieberkühn crypt depth) were analyzed before and after 60 days of including the enhanced probiotic mixture. For this procedure, samples (segments of the duodenum, jejunum, and ileum) were fixed in 10% formalin and analyzed using Hematoxylin-Eosin (H-E) staining, with morphometric changes evaluated through a digital trinocular microscope with 10X magnification. Finally, the productive parameters of the guinea pigs were recorded and analyzed.

2.4. Statistical Analysis

The collected data were analyzed using the R statistical software. First, a normality test was performed using the Shapiro-Wilk test to verify the distribution of the data. For each studied variable, including gastrointestinal pH, intestinal morphometry, and productive parameters, a one-way analysis of variance (ANOVA) was conducted to compare means among the three treatments (T1, T2, and T3). The composition of the gut microbiota was analyzed through frequency and prevalence analysis. Additionally, Pearson correlation analysis was used to assess the influence of pH on intestinal morphometric variables in each intestinal segment. Finally, a linear regression model was employed to investigate how independent variables (diet, gastrointestinal pH, and microbiota composition) affect dependent variables (productive parameters and intestinal morphometry). A value of p < 0.05 was considered statistically significant in all analyses.

3. Results

3.1. Gastrointestinal pH

The pH of the gastrointestinal tract in guinea pigs fed with different diets showed statistically significant differences (p<0.05) across the various segments analyzed. Guinea pigs fed an alfalfa-based diet had the highest pH in the stomach (5.88). In contrast, those fed a concentrate diet exhibited the highest pH values in the duodenum and jejunum, with readings of 7.13 and 8.38, respectively. No statistically significant differences (p>0.05) in pH were observed in the ileum and cecum based on the type of diet. The data are presented in Table 1.

3.2. Identification of the Intestinal Microbiota

A total of 17 bacteria were identified in the fecal microbiota of suckling guinea pigs, with Staphylococcus vitulinus and Escherichia coli being the most frequent. These bacteria belong to the Firmicutes and Proteobacteria phyla, respectively. In weaned guinea pigs integrated into treatments T2 and T3, a total of ten bacteria were identified, with Escherichia coli being the predominant bacterium. See Table 2 and Table 3.

3.3. Intestinal Morphometry

Statistical differences (p<0.05) were observed between treatments, and it was determined that age also influences the intestinal morphometric variables, with these variables increasing with age. Mixed feeding with the addition of 0.5% of the enhanced probiotic mixture (Probiolyte® WS) significantly increased the length of intestinal villi in the duodenum (537.83 µm) and ileum (293.64 µm) and the density of villi in the duodenum (67 per 4X field). Mixed feeding with the addition of 1% improved the width of intestinal villi in the duodenum (56.90 µm) and the depth of villi in the ileum (48.83 µm). Guinea pigs fed with concentrate increased the length of intestinal villi in the jejunum (433.70 µm) and the width in the ileum (51.87 µm). Concentrate feeding with the addition of 1% reinforced probiotic blend improved the depth of villi in the jejunum (52.93 µm). See Table 4.

3.4. Productive Parameters

The productive parameters (weight gain, feed intake, and feed conversion ratio) showed a significant difference (p < 0.05) between treatments. The guinea pigs fed with a mixed diet plus 0.5% of the reinforced probiotic blend reached the highest weight gain (284.67 g), the highest feed intake (1046.08 g), and the best feed conversion ratio (3.70) by the seventh week of the study, compared to the other treatments. See Table 5.

3.5. Correlation Analysis

The correlation analysis suggests that pH has a variable influence on the morphometric characteristics of intestinal villi depending on the segment of the digestive tract. In the jejunum and ileum, pH shows a stronger association with the length and width of the villi, whereas in the duodenum, the influence of pH is more limited. These findings highlight the importance of considering the specific segment when evaluating the impact of pH on intestinal morphometry. See (Table 6).

4. Discussion

4.1. Gastrointestinal pH

Previous studies on pH in the digestive system of guinea pigs and other species have reported varied results. For example, Merchant et al. [16] recorded a gastric pH of 2.9 in guinea pigs fed ad libitum, a pH in the small intestine ranging from 6.4 to 7.4, and pH values between 6.0 and 6.4 in the cecum and between 6.1 and 6.6 in the colon. Rechkemmer et al. [17] indicated that the pH of the jejunal microclimate in guinea pigs is 7.37, while the luminal pH is 7.27.
García et al. [18] demonstrated that pH influences the activity of amylolytic, cellulolytic, proteolytic, and lipolytic enzymes in the cecum of guinea pigs, observing lower cellulolytic enzyme activity at a pH of 5 and lipolytic activity at a pH of 9, without significantly affecting amylolytic and proteolytic activity. Pinchao et al. [19] reported that lactic acid bacteria (LAB) are more adaptable at intestinal pH levels of 2.9, 5.0, 6.4, and 7.4. On the other hand, Ramón [20] found that the pH in the stomach and cecum of guinea pigs performing cecotrophy is 1.53 and 6.63, respectively.
Vásquez et al. [8] measured pH in alpaca crias during the first 45 days of life, recording a gastric pH ranging from 6.91 to 5.95, and in the duodenum, jejunum, ileum, and cecum, pH values of 6.49 to 6.41, 6.64 to 6.71, 7.18 to 6.63, and 6.49 to 6.68, respectively. Gastrointestinal pH variations may be influenced by fiber levels in the diet, as high-fiber diets can neutralize some acidity by increasing saliva production, which is alkaline. The presence of certain minerals such as calcium and magnesium, as well as the amount and frequency of feeding, may also affect pH. Increased food intake may elevate hydrochloric acid production in the stomach, while long periods without feeding can reduce acidity. According to Miranda et al. [21], the inclusion of fermented bioadditives with lactic acid bacteria and yeasts produces organic acids (lactic and acetic acids) as metabolic byproducts, which can alter pH values along the gastrointestinal tract, Goichochea et al. [22] and thereby reduce bacterial growth, especially at pH equal to or below 4.

4.2. Identification of the Intestinal Microbiota

Different data from those found in this study have been reported by Frias et al. [23], who identified four phyla: Bacteroidota, Firmicutes, Spirochaetota, and Synergistota in the cecal microbiome of three guinea pig breeds: Andina, Inti, and Perú. The authors concluded that genetics could influence the structure and composition of the guinea pig cecal microbiome by finding unique genera for each breed.
On the other hand, Wu et al. [24] point to Ruminococcus_albus as the predominant bacterial community in the guinea pig intestinal microbiota. Meanwhile, Murga et al. [25] highlight Bifidobacterium longum (Phylum Actinomycetota), Fibrobacter succinogenes (Fibrobacterota), and Faecalibacterium prausnitzii (Bacillota), attributing that the composition or alteration of the microbiome may be related to the development of certain diseases or genetics. Zhu et al. [26] indicate that the addition of non-nutritive sweeteners (rebaudioside) to the diet of guinea pigs significantly alters the relative abundance of Lactobacillus.
Hildebrand et al. [27] demonstrated that the guinea pig intestinal microbiota is dominated by two phyla: Bacteroidetes and Firmicutes. Pinchao et al. [19] isolated 29 strains of lactic acid bacteria obtained from the intestines, cecum, and colon of adult and young guinea pigs, with Ligilactobacillus salivarius being the most prevalent strain; however, Alayande et al. [28] state that the origin of the intestinal microbiota is not well established.
These discrepancies between studies could be due to several reasons, including differences in methodologies used for bacterial identification, variations in diets and living conditions of the guinea pigs, and genetic diversity among different populations and breeds of guinea pigs. Additionally, it is important to consider the physiological state of the animals (infants, juveniles, or adults) and the impact of the immediate environment on the configuration of the microbiome.

4.3. Intestinal Morphometry

The results of the study differ from those reported by Carcelén et al., and Puente et al. [29,30], who added a probiotic mixture (Enterococcus hirae, Lactobacillus reuteri, L. frumenti, L. johnsonii, Streptococcus thoraltensis, and Bacillus pumilus) to a mixed diet (wheat bran plus forage) for guinea pigs, showing only benefits in the ratio of villi length to depth in the ileum and duodenum, respectively. Saccharomyces cerevisiae, added as a probiotic to the mixed diet of guinea pigs, also has a positive effect on villi width and the length of the crypt-villi axis.
Studies conducted on broiler chickens demonstrate the benefits of probiotics on intestinal morphometry; Roa et al. [31] report that the individual or mixed inclusion of probiotics (Saccharomyces cerevisiae, Lactobacillus sp., and Bacillus sp.) has a positive effect on the intestinal morphometry of the birds.

4.4. Productive Parameters

Several authors have studied the effect of additives such as probiotics, prebiotics, symbiotics, and enzymes on the diet of guinea pigs. Miranda et al. [32] assessed the impact of probiotics derived from a substrate of agro-industrial residues fermented with lactic acid bacteria and/or yeasts (Lactobacillus acidophilus, L. bulgaricus, Saccharomyces cerevisiae, and Kluyveromyces fragilis), with a molasses-vinasse substrate, and observed improvements in weight gain in guinea pigs. Andía & Lazo [33] report that the inclusion of a probiotic mixture of Lactobacillus acidophilus, L. casei, and Saccharomyces cerevisiae in the guinea pig diet has a significant effect on food consumption and carcass yield. Cuenca et al. [34] added garlic powder at 1%/kg of concentrated feed as a prebiotic and observed improvements in the productive parameters of guinea pigs starting from the third week of the experiment.
Contrarily, [29,35,36] report that the addition of probiotics, prebiotics, or symbiotics to guinea pig feed does not have a significant or consistent effect on the productive parameters of this species. Bazay et al. [37] indicate that mannan-oligosaccharides (MOS) included in the diet of guinea pigs during the fattening phase do not improve production parameters. Criollo et al. [38] report that the addition of Saccharomyces cerevisiae to the guinea pig diet does not have favorable effects on productive parameters.

5. Conclusions

The diet significantly influences gastrointestinal pH, intestinal microbiota, intestinal morphometry, and productive parameters in guinea pigs. These findings highlight the importance of diet composition and supplementation in the nutritional management of guinea pigs, with direct implications for optimizing their digestive health and productive performance. An optimal pH in the gastrointestinal tract promotes a balanced intestinal microbiota, which in turn positively impacts productive parameters and strengthens the immune system, emphasizing the interdependence of these factors in the health and performance of the animals.

Author Contributions

Conceptualization, Cuenca M. and Campos N.; methodology, Campos N, Cuenca M, Quinteros W.; software, Cuenca M.; validation, Cuenca M. and Campos N.; formal analysis, Cuenca M.; investigation, Cuenca M., Campos N. and Quinteros W.; resources, Cuenca M.; data curation, Cuenca M.; writing—original draft preparation, Cuenca M.; writing—review and editing, Cuenca M.; visualization, Campos N.; supervision, Cuenca M.; project administration, Cuenca M. Campos N.; funding acquisition, Cuenca M. All authors have read and agreed to the published version of the manuscript.

Funding

This research was funded by Catholic University of Cuenca-Ecuador, Department of Formative Research.

Data Availability Statement

Data are contained within the article.

Acknowledgments

Sixth cycle students of Veterinary Medicine - Catholic University of Cuenca-Ecuador, March-August 2024 cycle.

Conflicts of Interest

The authors declare no conflicts of interest.

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Table 1. Gastrointestinal pH Across Different Treatments.
Table 1. Gastrointestinal pH Across Different Treatments.
Treatments Stomach Duodenum Jejunum Ileum Cecum
T1. Alfalfa Diet 5.88b 5.75a 7.38ab 7.38a 7.25a
T2. Mixed Diet 5.00a 5.88a 6.75a 7.25a 6.75a
T3. Concentrate Diet 5.13a 7.13b 8.38b 8.25a 7.13a
p_Value 0.0195 0.0055 0.0066 0.1067 0.5397
a,b Values represent the mean pH measurements of each segment for guinea pigs fed with different diets. Statistical significance was assessed with a p-value < 0.05.
Table 2. Intestinal microbiota of lactating guinea pigs.
Table 2. Intestinal microbiota of lactating guinea pigs.
Microorganisms Frequency Prevalence
Staphylococcus vitulinus 4 13.3
Staphylococcus sciuri 3 10
Bacillus subtilis/amyloliquefaciens/vallismortis 2 6.7
Lysinibacillus fusiformis 1 3.3
Pantoea spp 1 3.3
Staphylococcus equorum 2 6.7
Bacillus cereus group. 2 6.7
Escherichia hermannii 1 3.3
Pseudomona putida 2 6.7
Paenibacillus thiaminolyticus 1 3.3
Bacillus licheniformis 1 3.3
Exiguobacterium acetylicum 1 3.3
Enterobacter cloacae 2 6.7
Escherichia coli 4 13.3
Staphylococcus gallinarum 1 3.3
Enterobacter ludwigii 1 3.3
Siccibacter turicensis 1 3.3
30 100
Table 3. Intestinal microbiota of guinea pigs supplemented with a reinforced probiotic mixture
Table 3. Intestinal microbiota of guinea pigs supplemented with a reinforced probiotic mixture
Microorganisms Frequency Prevalence
Escherichia coli 13 48.1
Micrococcus luteus 3 11.1
Acinetobacter lwoffii 3 11.1
Staphylococcus cohnii ssp urealyticus 2 7.4
Serratia liquefaciens 1 3.7
Staphylococcus xylosus 1 3.7
Lysinibacillus fusiformis 1 3.7
Staphylococcus equorum 1 3.7
Bacillus licheniformis 1 3.7
Acinetobacter johnsonii 1 3.7
27 100
Table 4. Intestinal microbiota of guinea pigs supplemented with a reinforced probiotic mixture.
Table 4. Intestinal microbiota of guinea pigs supplemented with a reinforced probiotic mixture.
Treatments
Segment Variable Phase Alfalfa Mixed Mixed 0.5% Mixed 1% Concent. Concent. 0,5% Concent. 1% p-Valor
Duodenum Length (µm) 1 353.98abcd 319.33ab 349.79abcd 335.73abc 333.40abc 317.13ab 353. 98abcd 0.00356
2 462.27bcde 456.70de 537.83e 410.10bcde 428.77cde 303.57a 442.06de
Width(µm) 1 34.77abc 38.87abcde 39.57abcdef 36.83abcd 34.27ab 34.20a 34.77abc 0.0072
2 41.43abcde 49.80ef 45.23cdef 56.90f 47.57def 38.47abcde 42.35bcdef
Depth (µm) 1 36.80a 34.53a 41.67a 39.80a 41.97a 38.83a 36.80a 0.2121
2 38.50a 39.17a 34.27a 33.17a 36.07a 36.83a 38.57a
Density 1 32.67a 33.67ab 33.67ab 32.67a 34.00ab 34.00ab 35.00abc 0.0006
2 62.00d 58.00d 67.00d 46.00abcd 56-00cd 51.00bcd 44.00abcd
Jejunum Length(µm) 1 213.06abcde 199.67abcd 166.20a 173.91a 181.38ab 182.69abc 213.06abcde 0.004
2 49.87de 272.10bcde 284.07bcde 293.77cde 433.70e 426.70e 403.67e
Width(µm) 1 35.07ab 32.73a 38.50c 35.03bc 37.40abc 32.37a 35.07ab 0.0061
2 37.50a 45.33a 46.90a 39.13a 43.40 a 40.30a 34.52a
Depth (µm) 1 35.10ab 35.83ab 36.23ab 33.17a 37.73abc 36.60ab 35.10ab 0.0022
2 52.37d 43.97bcd 42.53abcd 50.40 cd 46.23bcd 49.50cd 52.93d
Density 1 37.00a 37.00a 37.00a 37.00a 37.00a 41.00ab 36.00a 0.0006
2 53.33bc 62.00c 62.00c 62.00c 56.00bc 50.00abc 42.00abc
Ileum Length(µm) 1 208.82a 214.77ab 213.88ab 208.53a 209.58a 216.01ab 208.82a 0.0018
2 213.77ab 219.60abc 293.64cd 210.70ab 245.30abcd 213.97ab 283.80bcd
Width(µm) 1 33.80a 36.07a 32.13a 33.87a 36.20a 40.37a 33.80a 0.0001
2 38.17ab 48.53cd 36.70a 45.97bcd 51.87d 51.07d 41.07abc
Depth (µm) 1 38.57a 39.17a 34.27a 33.17a 36.07a 38.83a 38.57a 0.0516
2 45.50a 43.43a 41.00a 48.83a 44.23a 40.57a 48.25a
Density 1 43.67a 43.67a 43.67a 43.67a 43.67a 43.67a 43.67a 0.0055
2 57.33abc 68.00c 53.00abc 58.00bc 61.00bc 48.00ab 57.00abc
Means with a common letter are not significantly different (p > 0.05).
Table 5. Productive Performance of Experimental Guinea Pigs.
Table 5. Productive Performance of Experimental Guinea Pigs.
Age Weeks T1 Alfalfa T2 Mixed T2 Mixed (0,5%) T2 Mixed (1%) T3 Concentrated T3 Concentrated (0.5%) T3 Concentrated (1%) p-Value
Weight Gain (g) 4 110.00a 108.67a 116.00a 144.33a 121.33a 119.33a 98.33a 0.0929
5 131.33a 123.67a 146.33a 161.67a 131.00a 165.67a 134.33a 0.1855
6 79.67a 153.67a 171.00a 186.33a 154.67a 197.67a 167.33a 0.0962
7 217.33a 228.00a 284.67b 200.33a 212.33a 224.00a 184.67a 0.0004
Feed Intake (g) 4 511.33ab 435.23ab 506.80ab 584.73b 379.03a 537.13a 407.53a 0.0125
5 586.03a 578.56a 657.72a 709.67a 520.67a 703.65a 527.63a 0.0185
6 699.59ab 691.88ab 772.24ab 838.27b 649.04a 857.92b 634.48a 0.0049
7 929.32abc 901.60abc 1046.08c 986.83abc 812.28a 1020.45bc 836.08ab 0.0070
Feed Conversion 4 4.63b 4.00ab 4.33ab 4.10ab 3.17a 4.57b 4.13ab 0.0254
5 4.50a 4.67a 4.47a 4.43a 4.00a 4.33b 3.97a 0.5156
6 3.90a 4.53a 4.50a 4.50a 4.20a 4.37a 3.83a 0.0915
7 4.33ab 4.00ab 3.70a 4.93b 3.87ab 4.57ab 4.57ab 0.0167
Means with a common letter are not significantly different (p > 0.05).
Table 6. Correlation between gastrointestinal pH and intestinal morphometry.
Table 6. Correlation between gastrointestinal pH and intestinal morphometry.
Segment Variable pH
Duodenum Length − 0.146
Width 0.202
Depth 0.033
Density − 0.256
Jejuni Length 0.736
Width -0.015
Depth 0.114
Density -0.383
Ileum Length 0.619
Width 0.539
Depth 0.016
Density -0.200
Correlations between pH and intestinal morphometric variables (length, width, depth, and density of the villi) in different segments of the digestive tract of guinea pigs (duodenum, jejunum, ileum).
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