Characterization of Macroscopic and Microscopic Lesions of the Respiratory System of Guinea Pig (Cavia Porcellus) in Colombian Production Systems

doi:10.21203/rs.3.rs-4344466/v1

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Characterization of Macroscopic and Microscopic Lesions of the Respiratory System of Guinea Pig (Cavia Porcellus) in Colombian Production Systems

https://doi.org/10.21203/rs.3.rs-4344466/v1

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The guinea pig (Cavia porcellus), a hystricomorphic mammal raised by the inhabitants of southern Colombia, Ecuador, Perú and Bolivia, is a food of high nutritional, cultural and spiritual value in the Andean countries. Considering that there is no information on the characterization of respiratory pathologies in the guinea pig destined for human consumption in Colombia, the objective of the study was to characterize lesions and pneumonic patterns in the respiratory system. A cross-sectional observational study was carried out in guinea pigs (n = 270) of three weeks of age from 71 guinea pig farms distributed in 14 villages of the municipality of Pasto. In the animals included in the study, lesions in the nasal cavity and respiratory tract were evidenced in a percentage of less than 5%. In the pulmonary functional parenchyma, lesions were observed in 73.3% of the animals. Lymphocytic interstitial pneumonia was the most common finding − 36.6% (n = 99), followed by lymphohistiocytic interstitial pneumonia − 21.4% (n = 58) and multifocal granulomatous pneumonia − 3.7% (n = 10). Animals with concurrence of two morphological patterns of lesion in the same tissue were identified. No bronchointerstitial pneumonic patterns were found. It is concluded that respiratory alterations have a high occurrence (more than 70%) in the guinea pig population in the municipality of Pasto, Colombia. It is evident that most of the pneumonic patterns have a systemic entrance, which highlights the need to carry out new studies to have a more detailed understanding of the etiologies causing pneumonia in guinea pigs.

diagnosis

pneumonia

histopathology

epidemiology

respiratory disease

South America

farm animals

pneumonic patterns

In Colombia, guinea pig production as a source of food for human consumption is centered in the departments of Cauca, Putumayo and Nariño, the latter being the largest producer with more than 89% of national production and an estimated population of more than 900,000 animals, making it the third most important economic sector in the department's agricultural sector after livestock and agriculture¹⁸. In Nariño, it is estimated that there are 20,000 small farms, where 60% of them are concentrated in the municipality of Pasto¹⁶. This production is carried out under the following production systems: artisanal, artisanal-commercial and technified⁹. Regarding the diseases of this species, it has been reported that the pathologies that produce the highest mortality rates are those originating in the gastrointestinal tract and respiratory system⁴¹. However, most of these reports have been made on strains used for research and pets, with little information on diseases affecting guinea pig production systems intended for human consumption.

Due to the scarce information regarding the macroscopic and microscopic characterization of respiratory pathologies together with the high presentation of diseases of the respiratory system in guinea pig production systems⁴⁰, the objective of this study is to perform the anatomopathological characterization of the lesions of the nasal cavity, respiratory tract, and lungs of guinea pigs (Cavia porcellus) from traditional and technified exploitation systems in the municipality of Pasto.

Study design and population

An observational cross-sectional study was conducted on three-week-old guinea pigs (Cavia porcellus) from 71 production systems located in 14 villages in the municipality of Pasto, Colombia.

Sample size and sampling

The sample size was estimated assuming a finite population, based on the total guinea pig population reported for the Municipality of Pasto according to the 2016 Technical Bulletin of the National Agricultural Survey¹⁶. The guinea pig population reported in the department of Nariño was 1,057,235 animals, of which, the municipality of Pasto concentrates 60%^9,10 corresponding to 634,341 individuals. The sample size was calculated considering a confidence level of 95%, an expected proportion of 50% (the prevalence of respiratory diseases in guinea pigs in the municipality of Pasto is not known) and a precision level of 6% using the formula described by Thrusfield³⁹.

$$n= \frac{N \times {Z\alpha }^{2} \times p \times q}{{e}^{2} \times \left(N -1\right) + {Z\alpha }^{2} \times p \times q}$$

N = Total population reported (634,341 guinea pigs).

Zα = 1.96 for a confidence level of 95% (α = 0.05).

P = proportion of respiratory diseases (50%).

q = 1- p.

e = accuracy of the study 6%.

Based on these criteria, a sample size of 266 animals was obtained. The calculated sample size was increased by 3% (correction factor) considering data and animal losses during the study. The total number of animals to be evaluated was 270.

Inclusion criteria: three-week-old apparently healthy male and female animals, belonging to the rearing stage according to the productive parameters described by Chauca; Caicedo and Huamán^19,14,21, from livestock farms of guinea pig producer associations, registered by the Secretariat of Agriculture of the Municipality of Pasto³⁵.

Sampling: since, in the Municipality of Pasto, the distribution of the study population varies in each village^17,35 a stratified sampling by proportional allocation was carried out in each village. Four animals were randomly taken per farm following the proportion of the guinea pig population in each village as described in Table 1.

Table 1

Distribution of townships in the municipality of Pasto of guinea pig (*Cavia porcellus*) producer associations and number of animals to be sampled.
District	Animals per farm	% of population	Sampled farms
Catambuco	40	27%	10
El encano	40	27%	10
La caldera	32	21,6%	8
Mocondino	26	17,55%	7
Cabrera	22	14,85%	6
San Fernando	20	13,5%	5
La laguna	18	12,15%	5
Santa Bárbara	18	12,15%	5
Mapachico	10	6,75%	3
Jamondino	10	6,75%	3
Obonuco	8	5,4%	2
Jonjovito	8	5,4%	2
Genoy	6	4,05%	2
Morasurco	12	8,1%	3
Total	270	100%	71

Sample collection and processing

The animals were selected at each farm by a person outside the study, who chose the individuals at random, apparently healthy (without evident clinical signs of disease) to guarantee the heterogeneity of the sample and minimize biases¹³. Subsequently, they were transferred from the different farms to the necropsy room of the Carlos Martínez Hoyos Veterinary Clinic of the University of Nariño - Colombia.

The animals were anesthetized using an inhalation anesthesia equipment for use in small animals; for this purpose, the guinea pigs were placed in a hermetically sealed container to which isoflurane was insufflated at a concentration of 4% until the animals were induced in the anesthetic plane. Finally, euthanasia was performed by intracardiac administration of sodium pentobarbital (390 mg/ml) in combination with sodium diphenylhydantoin (50 mg/ml), at a dose of 200 mg/kg. Subsequently, the necropsy procedure was performed.

Macroscopic evaluation

for the evaluation of the nasal cavity, airways and lungs, the trachea, bronchi, and lungs were completely excised. For the evaluation of the nasal cavity, the atlanto-occipital joint was disarticulated, and the skin and integument were removed and fixed together with the other organs in 10% buffered formalin for 48 hours.

Prior to fixation, each individual underwent a photographic record and preliminary macroscopic morphological diagnosis of the alterations in the lung parenchyma, taking into account the distribution pattern of lung lesions established by Caswell and Williams¹².

Microscopic evaluation: Transverse cuts were made with a 0.3cm thick manual hair saw from the nasal cavity of four anatomical segments referenced as segment T1, T2, T3 and T4. Each cutting segment was established as follows: 1) Segment T1: anatomical landmark (posterior upper incisor teeth); 2) Segment T2: anatomical landmark (incisive papilla); 3) Segment T3: anatomical landmark (second palatal ridge); 4) Segment T4: anatomical landmark (first molar tooth).

The anatomical landmarks were based on those described by for experimental studies of the respiratory system in laboratory animals^28,33. The sections were deposited in a decalcifying solution of 10% buffered formalin and 20% formic acid for ten days. Finally, they were embedded in paraffine and hematoxylin and eosin staining was performed (H&E). The anatomical regions for the microscopic evaluation of each transversal section of the nasal cavity corresponded to the middle septum, dorsal septum, ventral septum, turbinate and submucosa glands as described by Botero¹⁷.

The trachea was sectioned twice transversally as described by Morawietz²⁸. Subsequently, parafifin embedding and hematoxylin and eosin staining were performed. The lower airways (bronchi and intrapulmonary bronchioles and the lung parenchyma were sectioned according to Guidance Document on Histopathology for Inhalation Studies, Morawietz and Adner^1,28,33 as follows: 1) right cranial lung lobe a complete horizontal cut; 2) right middle lung lobe a complete horizontal cut; 3) right accessory lung lobe a complete diagonal cut; 4) left lung: a complete diagonal cut.

Finally, the tissues were embedded in paraffin and stained with hematoxylin and eosin stain.

Classification of lesions

The macroscopic and microscopic findings in the respiratory system reported in guinea pigs^{,5,8,20,29,34,43} and histologically described in rodents cited by Scundamore and Treuting^25,27 was taken as reference. Evaluation of the eleven histological tissue sections per individual was performed on a Nikon Eclipse E-200-LED optical microscope at 40X, 100X and 400X magnifications.

The presence of microscopic lesions was established based on what is published in the international guide for harmonization of the nomenclature of toxicological pathology in rodents²⁶ and the published guide for proliferative and non-proliferative lesions in rodents³² adjusted to the microscopic particularities of the guinea pig described by Barthold⁴. Based on this, each lesion was identified, and a semi-quantitative scale of severity was estimated and adjusted based on that established by Mann²⁶ as described in Table 2, categorizing each lesion into "mild", "moderate" and "severe". Finally, the morphological diagnoses of each tissue and their corresponding severity scale were established.

Table 2

Grading system for lesion determination and morphological diagnoses.
Numeric Score	Description	Definition
0	Normal	Tissue considered normal, under the conditions of the study and considering the age, sex, and strain of the animal. Alterations may occur that in other circumstances would be considered deviations from normality.
1	Mild	In general, the injury is easily identifiable, but of limited severity.
2	Moderate	The lesion is prominent, but there is significant potential for increased severity.
3	Severe	The degree of change is as complete as possible (occupying most of the organ).

An animal was considered to be free of microscopic lesions and respiratory pathology when histologically normal tissues were observed in the microscopic analysis as described by Scundamore and Treuting^25,27. Each histological micro preparation of each study individual was randomly evaluated using the methodology of concealment to the investigator.²²This procedure was repeated twice.

Statistical analysis

Study variables. Macroscopic alterations, histopathological changes in nasal cavity, upper and lower airways, pneumonic patterns, type of distribution and degree of severity.

A descriptive analysis was performed using frequency tables to determine the percentage of each variable in the study population. The Stata 18.0 statistical package was used for data analysis.

Bioethics Committee

The project was endorsed and approved by the bioethics committee of the FMVZ of the National University of Colombia - Bogotá D. C., through minute No.07 of 2017.

Gross Pathology

In the study in the 270 animals, no macroscopic alterations were evident in the nasal cavity, trachea or respiratory tract. As for the lung tissue (Fig. 1), no macroscopic lesions were evident in 81.48% (n = 220) of the cases. Table 3 reports the macroscopic findings.

Table 3

Macroscopic findings in lung parenchyma in guinea pigs (n = 270) from 71 farms located in the Municipality of Pasto, Colombia.
Finding	Frequency	%
Apparently normal	220	81.48
Embolic pneumonia	38	14.07
Interstitial pneumonia	10	3.7
granulomatous pneumonia	2	0.74

Microscopic evaluation

Nasal cavity, trachea and extrapulmonary upper airways

In 259 animals (95.9%) no alterations were evidenced in the four cross sections of the nasal cavity. Rhinitis was reported in 4% of the individuals (n = 11).

Lung parenchyma

A general description of the findings is shown in Fig. 2.

Of the animals evaluated, 73.7% presented histopathological alterations in the pulmonary parenchyma. A total of 16 types of morphological diagnoses with different degrees of severity, chronicity and distribution pattern were identified (Fig. 3).

Lymphocytic interstitial pneumonia was the most common finding with 36.6% (n = 99), followed by lymphohistiocytic interstitial pneumonia − 21.4% (n = 58), granulomatous multifocal pneumonia − 3.7% (n = 10). Animals with concurrence of two morphological patterns of lesion in the same tissue were observed, being granulomatous interstitial and multifocal granulomatous pneumonia the most common concurrence − 6.6% (n = 18 cases). The remaining pneumonic patterns presented percentages less than 1% (n ≤ 2). Two individuals presented interstitial lung disease (diffuse alveolar damage) in exudative stage; this finding is attributed to ventilation-induced lung injury in the euthanasia procedure¹¹. In the study, no evidence of bronchointerstitial pneumonic patterns was found.

Regarding severity (Fig. 3), the lesions were categorized as mild, moderate and severe according to the methodology. It was found that 14.57% (n = 29) were classified as mild, 41.70% (n = 83) as moderate and 43.71% (n = 87) as severe. Regarding chronicity, the study showed that 99% of animals with alterations in the pulmonary functional parenchyma (n = 197) were chronic in nature and two individuals (1%) presented acute lesions.

Regarding the morphological pattern of distribution, the study showed that the interstitial type was the most common, followed by the multifocal granulomatous pattern. About the route of admission, it is important to mention that the study showed that in 70% of the cases, events distant to the lung of systemic origin, some of possible infectious origin, were the ones that gave rise to pneumonia. Table 4 reports additional findings in lung parenchyma.

Table 4

Pneumonic patterns (other microscopic findings) in guinea pigs (n = 270) from 71 farms located in the Municipality of Pasto, Colombia.
Disturbance	Category	Frequency	%
Pulmonary vasculitis	Present	0	0,0
Pulmonary vasculitis	Absent	270	100
Type II pneumocyte proliferation	Present	0	0,0
Type II pneumocyte proliferation	Absent	270	100
Hyaline membranes	Present	268	99,2
Hyaline membranes	Absent	2	0,8
Fibrosis	Present	269	99,6
Fibrosis	Absent	1	0,4
Left Heart Failure Cells	Present	0	0,0
Left Heart Failure Cells	Absent	270	100
Coagulation necrosis	No	270	100
	Mild	0	0,0
	Moderate	0	0,0
	Severe	0	0,0
Caseification Necrosis	No	270	100
	Mild	0	0,0
	Moderate	0	0,0
	Severe	0	0,0
Diffuse Alveolar Damage	Present	2	0,7
Diffuse Alveolar Damage	Absent	268	99,3
Pulmonary thrombosis	Present	1	0,4
Pulmonary thrombosis	Absent	269	99,6
Entrance route	Not determined	82	30,3
	Aerogenic	0	0,0
	Hematogenous	188	69,7
	Aerogenic and hematogenous	0	0,0

In relation to possible etiological agents involved in the histopathological diagnoses. Staphylococcus aureus was isolated in 8 cases corresponding to 2.96%, corresponding to cases with a diagnosis of lymphocytic interstitial pneumonia, four cases with lymphocytic interstitial and multifocal granulomatous pneumonia of systemic origin, one case with multifocal granulomatous pneumonia and one case with multifocal pyogranulomatous pneumonia (Table 5).

Table 5

Positive histopathological and microbiological diagnoses in functional lung parenchyma in guinea pigs (n = 270) from 71 farms located in the Municipality of Pasto, Colombia.
Morphological diagnosis	Isolated microorganism	Frequency	%
Lymphocytic interstitial N.	Staphylococcus aureus	2	25
Lymphocytic and granulomatous interstitial N.	Staphylococcus aureus	4	50
	Staphylococcus aureus	1	12.5
Multifocal Granulomatous N.	Staphylococcus aureus	1	12.5
Total		8	100

Regarding the type of inflammatory infiltrate present, it was predominantly of mononuclear type; within this, the one composed of lymphocytes corresponds to the highest percentage of presentation, followed by the granulomatous infiltrate. The cellularity (Fig. 4) presented variations in terms of its form, being 93.81% conformed by lymphocytes, histiocytes and macrophages. Lymphocytes, macrophages, histiocytes and giant cells made up 5.15% and lymphocytes and histiocytes 1.03%.

Pleuritis, vasculitis in pulmonary arteries and veins, cardiac failure cells, type II pneumocyte hyperplasia, extensive foci of changes associated with cell death and cytopathic effect in airway epithelium were not evidenced in any animal.

The study is the first exploratory descriptive work focused on determining upper respiratory lesions and pneumonic patterns from a representative sample of the guinea pig population of the municipality of Pasto, which corresponds to 65% of the population of Colombia. Descriptive cut-off investigations provide valuable information on the status of different types of health events in a specific population¹³.

Although the guinea pig is widely used as a model for the study of nasal cavity pathologies^3,42. The research showed an occurrence of lesions in the nasal cavity and extrapulmonary upper respiratory tract of less than 5%. Represented in rhinitis with eosinophilic inflammatory component of allergic type according to the classification cited by Liva²³. These results suggest that pathologies in the nasal cavity and trachea may not have a high impact on the population under the management conditions of guinea pig production systems in Pasto. Garcia and collaborators report that in a study of necropsies of 1000 animals they found a prevalence of 4% of pathologies in the nasal cavity². For this reason, prospective and cohort studies with a population sample in different age ranges and longer periods of exposure to possible risk factors are recommended to determine the true incidence of respiratory disease in the upper respiratory tract of guinea pigs.

The population selected for this study corresponded to apparently healthy male and female guinea pigs of 3 weeks of age (in the rearing stage). We worked with this sample because we did not find information related to prevalence of respiratory pathologies in Colombia and for this reason, we decided to study a uniform population with a defined age range. Additionally, different authors mention that at this age, individuals may be more prone to contract diseases because at this stage of the productive cycle, stressful events such as separation from the mother, deprivation of maternal milk intake, transfer to the cage or pen, sexing, among others, occur. These situations could be considered as potential factors favoring the development of respiratory pathologies ^{14,15,30,37,41}. However, the study did not find bronchointerstitial pneumonias with cytopathic changes in the respiratory epithelium. These findings highlight the need to replicate this study model in neonatal animals and kits in the first weeks to determine if concomitant involvement of possible viral agents is evident in the respiratory disease of guinea pigs destined for production.

Regarding macroscopic pneumonic patterns. The embolic pattern was the most easily identified and had the highest degree of concordance with respect to the microscopic evaluation, 14.07% versus 11.04%. However, the interstitial pattern with 3.7% was underrepresented in the macroscopic evaluation, when compared with the microscopic findings where it corresponded to more than 80% of the cases. These results show that this diffuse pattern is not always easily recognized macroscopically by the pathologist. This information is similar to that mentioned by Carvallo and Stevenson in domestic animals¹¹; additionally, the lung tissue evaluated corresponds to that of small hystricomorph rodents, which can generate greater difficulty in its identification and therefore, generates that the lesion goes unnoticed at the time of evaluation. These findings are consistent with those reported in a descriptive study of pneumonia in guinea pigs in Peru by Villanueva-Guzmán⁴⁰. Finally, multifocal granulomatous and embolic pneumonia also presented a higher degree of concordance with respect to microscopic findings with 14.81% versus 11.04%.

The investigation found in general terms a high occurrence of well-defined and categorized pneumonic lesions and patterns in the pulmonary functional parenchyma with different degrees of severity in 73.3%. Data like those reported by Garcia². They state that respiratory disease, particularly pneumonia, in these species may present a subclinical course and may be underdiagnosed. They mention that, in guinea pig necropsies at their diagnostic center, 65% of animals present some type of respiratory pathology at the time of death, with interstitial pneumonia being the most prevalent finding. Information similar to that reported by Villanueva⁴⁰ who report a prevalence of 75% in their study. We share the opinion of the authors mentioned above, whose data on the frequency of pneumonia presentation are like those found in the present study. On the other hand, another possible explanation may be associated with the ethological characteristics of the guinea pig, being prey animals, they try to mask clinical signs and disease states^7,36,38 which causes respiratory pathologies in the field to be underdiagnosed.

Carvallo and Stevenson¹¹ define interstitial pneumonia as a term used to describe a wide range of infectious (e.g., viral) and non-infectious (e.g., toxic) interstitial diseases, or to describe the increased number of leukocytes in the alveolar septa. The results of the study open the door to a wide field of research for the approach of specific interdisciplinary studies to have a better understanding of each of the possible etiologies of interstitial pneumonia in guinea pig. The role of histopathology in the diagnosis of interstitial lung diseases is fundamental but it is not everything; because lung responds to lesions in a limited number of ways (i.e., "lesion patterns'') associated with the similarities in lesion patterns among the different causes that produce interstitial pneumonia make diagnosis challenging when based solely on a histopathological description³¹. This highlights the need for constant collaborative work between different medical disciplines.

Another representative pneumonic morphologic pattern of lesion evidenced in the study corresponded to multifocal with 14.6%, with predominantly granulomatous inflammatory cellularity. These findings denote a possible gateway of origin to systemic events distant to the chronic lung²⁴. Paz in a descriptive study of pathologies in the intestinal tract carried out from a statistically representative sample of the region found a 100% prevalence of lesions of granulomatous nature with different degrees of severity in the small intestine, large intestine, and liver³⁰. These findings could suggest that there is possibly some relationship between digestive pathologies and granulomatous morphological patterns in the lung. Therefore, it would be interesting to perform descriptive morphological studies correlating the lung with lesions in different physiological systems of the guinea pig.

In sum, the research shows that pulmonary pathologies can represent a high health, economic and productive impact on guinea pig farms in the municipality of Pasto and highlights the importance of continuing with prospective studies focused on determining the incidence, etiology, and causality of guinea pig lung disease in the region.

Author Contributions: C.CH performed necropsy, methodological design, macroscopic and microscopic analysis of tissues from the study animals; L.B contributed to methodological design of the research. T.P contributed to performing necropsies, sampling, and processing slides.

Declaration of Conflicting Interests: the authors declare that they have no conflict of interest with respect to the research, authorship and/or publication. This research received no specific grant from any funding agency in the public, commercial, or not- for-profit sectors.

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No competing interests reported.

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Characterization of Macroscopic and Microscopic Lesions of the Respiratory System of Guinea Pig (Cavia Porcellus) in Colombian Production Systems

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Abstract

Figures

Introduction

Materials and methods

Study design and population

Sample size and sampling

Sample collection and processing

Classification of lesions

Statistical analysis

Bioethics Committee

Results

Gross Pathology

Microscopic evaluation

Lung parenchyma

Discussion

Declarations

References

Additional Declarations

Status:

Version 1