Assessment of studies on oral manifestations and COVID-19: a meta-research study

Introduction

World Health Organization (WHO) declared a global pandemic for COVID-19 in early 2020. The rapid spread of the disease caused by the SARS-CoV-2 virus brought the need to produce quick answers on the topic, generating a substantial number of articles. In dentistry, it was no different. In the first year of the pandemic, more than one thousand five hundred articles were published in the PubMed database about “COVID-19 and Dentistry”¹. Despite the urgency of knowledge, this mass production also generated concern in the scientific community about the quality and accuracy of these studies².

The oral mucosa is one of the entry routes for SARS-CoV 2, arising from human salivary gland receptors, believing that oral symptoms such as loss of smell, taste, and xerostomia, may be precursor symptoms of COVID-19, even before the typical clinical symptoms³. Thus, the clinical picture pattern of this disease may include oral signs and symptoms⁴. A living systematic review, which aims to be updated every six months, reported in its first publication in 2020 that the most prevalent symptom was taste alteration⁵. In their last update, published in 2021, the authors analyzed an increase in the publication of studies on the topic and the most prevalent oral symptom, up to that point, was xerostomia, followed by taste alterations⁶. However, afterward, a cohort study of 154 patients positive for viral disease reported that the most prevalent oral manifestation was oral ulcers⁷, disagreeing with the results of previous systematic reviews⁵,⁶.

Despite there are systematic reviews on this topic, most of the primary studies published diverge methodologically, assessed the prevalence of oral lesions as secondary outcomes⁸, presenting a lack of a plausible understanding of the establishment of the causal relationship between oral conditions and the virus⁶, and the diagnostic methods are not standardized which can jeopardize the understanding of this subject. Therefore, considering that previous literature presents different study designs involving COVID-19 and the oral manifestations with different results, this study aimed to evaluate how different study designs influences the presence and characteristics of diagnosis of oral manifestations in patients with COVID-19.

Methodology

This a meta-search study conducted with studies evaluating the relationship between patients with oral manifestations and COVID-19. The protocol for this study was previously registered with OSF Registries (https://doi.org/10.17605/OSF.IO/MS2ZF).

Eligibility criteria

We included studies published in scientific journals with adult subjects, with no maximum age restriction, who tested positive for COVID-19 through a confirmatory diagnostic test, which may be the results of the SARS-CoV-2 polymerase chain reaction (PCR) or other, and who reported some type of oral lesion, regardless of how this lesion was diagnosed. Original studies of any design such clinical trials, observational studies and case-reports were included. However, review articles, letters to the editor, and pilot studies were excluded. Due to financial constraints, only studies in the English language were included. Review articles, letters to the editor, and pilot studies were excluded.

Search strategy

Searches were conducted in the electronic databases PubMed, Scopus, and Web of Science from January 1, 2020 (corresponding to the first reported cases of the disease worldwide) to November 1, 2022. The search strategy was designed for PubMed, based on Mesh terms and keywords, and after, adapted for the Scopus and Web of Science databases (full search strategies could be found in supplementary table 1). The references cited in the included articles were also reviewed to identify other relevant studies.

Supplementary table 1
. Search strategy

PubMed

(( “oral manifestations”[MeSH Terms] OR “oral manifestation” OR “oral lesion” OR “oral lesions” OR “oral mucosal lesion” OR “oral mucosal lesions” OR “mucocutaneous lesions” OR “oral alteration” OR “oral alterations” OR “pathology. oral”[MeSH Terms] OR “oral pathology” OR “oral pathologies” OR “oral complication” OR “oral complications” OR “oral change” OR “oral changes” OR “mouth diseases”[MeSH Terms] OR “mouth disease” OR “oral disease” OR “oral diseases” ) AND (( “2019 nCoV” OR 2019nCoV OR “2019 novel coronavirus” OR “COVID 19” OR COVID19 OR “new coronavirus” OR “novel coronavirus” OR “SARSCoV-2” OR “COVID-19” OR “SARS-CoV” OR “2019-nCoV” OR “SARS-CoV-2” OR “coronavirus” OR coronavirus OR COVID OR SARS)

Scopus

( TITLE-ABS-KEY ( “oral manifestations” OR “oral manifestation” “ OR “oral lesion” OR “oral lesions” OR “oral mucosal lesion” OR “oral mucosal lesions” OR “mucocutaneous lesions” OR “mucocutaneous viral lesions” OR “oral alteration” OR “oral alterations” OR “oral pathology” OR “oral pathologies” OR “oral complication” OR “oral complications” OR “oral change” OR “oral changes” OR “mouth diseases” OR “mouth disease” OR “oral disease” OR “oral diseases” ) AND TITLE-ABS-KEY (“2019 nCoV” OR 2019ncov OR OR “2019 novel coronavirus” OR “COVID 19 OR covid19 OR “new coronavirus” OR OR “novel coronavirus” OR “SARS CoV-2” OR covid-19 OR sars-cov OR 2019-ncov OR sars-cov 2 OR coronavirus OR covid OR sars))

Web of Science

TS= (oral manifestations OR oral manifestation OR oral lesion OR oral lesions OR oral mucosal lesion OR oral mucosal lesions OR mucocutaneous lesions OR mucocutaneous viral lesions OR oral alteration OR oral alterations OR oral pathology OR oral pathologies OR oral complication OR oral complications OR oral change OR oral changes OR mouth diseases OR mouth disease OR oral disease OR oral diseases) AND TS=(2019 nCoV OR 2019ncoV OR 2019 novel coronavirus OR COVID 19 OR covid19 OR new coronavirus OR novel coronavirus OR SARS CoV-2 OR covid-19 OR sars-cov OR 2019-ncov OR coronavirus OR covid OR sars OR sars-cov-2)

Selection process

After the search strategy, the studies were imported into the Rayyan QCRI program (https://rayyan.qcri.org) to perform duplicate article removal. A pilot test was conducted to test agreement in study selection between the reviewers involved in this phase. After, two reviewers independently reviewed the titles and abstracts of all studies. Articles meeting the eligibility criteria and those with insufficient data in the title and abstract were selected for full-text reading. Subsequently, the full-text reading was performed independently by the same two reviewers considering the same criteria once more. Discrepancies in selecting titles, abstracts, and full-text articles were resolved through discussion with a third reviewer until a consensus was reached.

Data extraction

For data collection, a standardized form was created using Excel software. Two reviewers analyzed the selected studies to test the data extraction and ensure consistency in the analysis and collection of information. Subsequently, one reviewer extracted the data from the included studies, and then the second reviewer checked the consistency of the data.

The following data were extracted: year of publication, first author name, the continent of study conduct, study design (randomized clinical trials, cross-sectional, cohort, case-control studies, case report or case series), diagnostic test for COVID-19 (PCR or other), presence and clinical presentation (signs and symptoms) of the oral lesion(s), time of manifestation of oral lesion symptomatology, and how the diagnosis of the oral lesion(s) was made (clinical examination, laboratory examination, teledentistry, or self-report). Case report was considered only when a single case was reported in the study, and case series were considered studies that reported two or more cases.

According to the eligibility criteria of this review, studies that had patients diagnosed with COVID-19 through a confirmatory test would be included. In contrast, some studies did not show this confirmation through a laboratory test, but rather the confirmation was through patient self-report. We chose not to exclude these studies because we believe it would be important to discuss the lack of standardization in confirming the disease.

Data analysis

Data were analyzed using Stata 14.0 software. Descriptive analysis was performed to assess the relationship between the oral manifestations and COVID-19 in the different study designs. In addition, a comparison analysis was performed between the oral manifestations of the lesions that appeared most in the studies (ulcer, taste alteration, xerostomia, candidiasis, periodontal disease, and herpes simplex), diagnosis of oral manifestations (clinical examination, laboratory examination, or self-report/tele odontology), and the study design. Taste alteration was considered anosmia, dysgeusia, or ageusia. Periodontal disease was the report of gingival or periodontal disease. Results are presented as frequency (n) and percentage (%).

Results

Figure 1 shows a flow chart summarizing the article selection process. The search initially yielded 2064 potentially relevant articles (PubMed: n = 1151; Scopus: n = 559; Web of Science: n = 354), after removing duplicates, 1486 articles were included based on title and abstract, and among these, 95 articles were included for reading the full text. Finally, 55 studies were included in the data synthesis analysis.

Figure 1
Flowchart of the selection process.

Supplementary Table 2 presents the list of included articles. The studies were conducted on four different continents, Asia (21 articles, 38.9%), America (14 articles, 25.9%), Europe (12 articles, 22.2%) and Africa (7 articles, 13.0%). Table 1 presents the characteristics of included studies. Most of the studies were case reports (n=21, 38.2%) and case series (n=13, 23.6%), and among the analytical observational studies, 10 studies were cohort and cross-sectional studies (18.2%), and 1 study was case control (1.8%).

Supplementary table 2
. Data extraction.

Year	Author	Continent	Design of study	Oral manifestation	Diagnosis of COVID-19	Diagnosis of oral lesion
2020	Amorim dos Santos et al.9	American	Case report	Ulcer e Taste alteration	PCR	Clinical examination.
2020	Brandão et al.10	American	Case series	Ulcer, Taste alteration, herpes	PCR	Laboratory examination.
2020	Corchuelo et al.11	American	Case report	Candidiasis, ulcer	PCR	Teledentistry and self-report.
2020	Cruz Tapia et al.12	American	Case series	Taste alteration, ulcer	PCR	Laboratory and clinical examination.
2020	Fantozzi et al.13	Europe	Cohort	Taste alteration, xerostomia	PCR	Self-report.
2020	Sinjari et al.14	Europe	Cohort	Taste alteration, xerostomia	N/A	Self-report.
2020	Zarch et al.15	Asian	Case report	Xerostomia, taste alteration, ulcer	PCR	Teledentistry.
2020	Biadsee et al.16	Asian	Case series	Xerostomia, Taste alteration	PCR	Self-report.
2020	Kitakawa et al.17	American	Case report	Ulcer	PCR	Clinical examination.
2021	Subramaniam et al.18	Asian	Case series	Ulcer, candidiasis, Taste alteration	PCR	Clinical examination.
2021	Gherlone et al.19	Europe	Cohort	Xerostomia, taste alteration	PCR	Clinical examination.
2021	Abdelgabar et al.20	Europe	Case report	Ulcer	PCR	Laboratory examination.
2021	Fisher et al.21	American	Case report	Edema	N/A	Laboratory examination.
2021	Favia et al.22	Europe	Cross-sectional	Ulcer	PCR	Laboratory examination.
2021	Saleh et al.23	African	Case report	Oral lichen planus	N/A	Laboratory and clinical examination.
2021	Naser et al.24	Asian	Cohort	Ulcer, necrosis, taste alteration, parotiditis	PCR	Clinical examination.
2021	Nejabi et al.25	Asian	Case report	Ulcer	PCR	Clinical examination.
2021	El Kady et al.26	African	Cohort	Taste alteration, xerostomia, candidiasis, Ulcer	PCR	Self-report.
2021	Carreras-Presas et al.27	Europe	Case series	Ulcer	N/A	Teledentistry.
2021	Eita et al.28	African	Case report	Taste alteration	PCR	Clinical examination.
2021	Katz29	American	Cross-sectional	Candidiasis	PCR	Self-report.
2021	Elamrousy et al.30	African	Cross-sectional	Taste alteration, xerostomia, candidiasis, ulcer	PCR	Clinical examination, Self-report.
2021	Abubakr et al.31	African	Cross-sectional	Halitose, ulcerações, xerostomia	PCR	Self-report.
2021	Natto et al.32	Asian	Cross-sectional	Taste alteration, periodontal desisases, ulcer	PCR	Self-report and clinical examination.
2021	Hocková et al.33	Europe	Case series	Ulcer, parotiditis	PCR	Clinical examination.
2021	Saleh et al.34	African	Case report	Ulcer, herpes zoster	N/A	Clinical examination.
2021	Teixeira et al.35	American	Case series	Ulcer, candidiasis	PCR	Clinical examination.
2021	Dalipi et al.36	Europe	Case report	Ulcer	PCR	Clinical examination.
2021	Fathi et al.37	Asian	Case report	Ulcer	PCR	Clinical examination.
2021	Ramires et al.38	American	Case report	Ulcer	PCR	Clinical examination.
2021	Nuño González et al.39	Europe	Cross-sectional	Edema, ulcer, mucositis	PCR	Clinical examination.
2021	Rai et al.40	Asian	Case series	Candidiasis, ulcer	PCR	Clinical examination.
2021	Jawanda et al.41	Asian	Case report	Mucormycose, Actinomicose, Candidiasis, Osteomyelitis	PCR	Laboratory examination.
2021	Khodavirdipour et al.42	Asian	Case series	Xerostomia, ulcer, Taste alteration	PCR	Clinical examination and self-report.
2022	Anand et al.43	Asian	Caso-control	Periodontal desiases	PCR	Clinical examination.
2022	Aswin et al.44	Asian	Case report	Mucormycose	N/A	Laboratory examination.
2022	Ganesan et al.45	Asian	Cross-sectional	Taste alteration, xerostomia, candidiasis, ulcer	PCR	Clinical examination.
2022	Yeom et al.46	American	Case series	Ulcer, candidiasis	N/A	Laboratory examination.
2022	Walsh et al.47	American	Cohort	Edema	N/A	Clinical examination.
2022	Palaia et al.48	Europe	Case report	Ulcer	PCR	Clinical examination.
2022	Koračin et al.49	Europe	Case report	Cheilitis	PCR	Laboratory examination.
2022	Hans et al.50	Asian	Cross-sectional	Taste alteration, ulcer	PCR	Teledentistry and self-report.
2022	Schwab et al.7	American	Cohort	Candidiasis, herpes	PCR	Laboratory and clinical examination.
2022	Reis et al.51	American	Cross-sectional	Taste alteration	PCR	Self-report.
2022	Poorna et al.52	Asian	Case report	Ludwig’ Angina	Other	Laboratory examination.
2022	Talahatu et al.53	Asian	Case report	Ulcer	N/A	Teledentistry.
2022	Dilsiz et al.54	Asian	Case report	Ulcer	PCR	Clinical examination.
2022	Eduardo et al.55	American	Cohort	Xerostomia, candidiasis	PCR	Clinical examination.
2022	Muthyam et al.56	Asian	Cross-sectional	Xerostomia, ulcer, Taste alteration	PCR	Self-report.
2022	Chawla et al.57	Asian	Cross-sectional	Xerostomia, Taste alteration, ulcer	PCR	Clinical examination and self-report.
2022	Al-Mahalawy et al.58	African	Case series	Osteonecrosis	PCR	Laboratory examination
2022	Tantawi et al.59	African	Cross-sectional	Xerostomia, Taste alteration	PCR	Self-report.
2022	Al-Ak’hali et al.60	Asian	Case report	Ulcer	PCR	Laboratory examination.
2022	Gebretsadik et al.61	African	Cohort	Ulcer, xerostomia, candidiasis	N/A	Clinical examination.
2022	Binmadi et al.62	Asian	Cohort	Taste alteration, xerostomia, candidiasis, Ulcer	Self-report	Teledentistry and self-report.

• PCR: polymerase chain reaction
• N/A: not available

Table 1
Descriptive analysis of the analyzed articles (n=55).

Year of COVID-19 diagnosis	n (%)
2020	9 (16.4)
2021	25 (45.5)
2022	21 (38.1)
Study design
Case report	21 (38.2)
Case series	13 (23.6)
Cross-sectional	10 (18.2)
Cohort	10 (18.2)
Caso-control	1 (1.8)
Diagnosis of Covid-19
PCR*	42 (76.4)
Other	03 (5.4)
Not done/not available	10 (18.2)
Diagnosis of oral manifestations
Clinical examination	24 (43.6)
Laboratory examination	13 (23.6)
Patient self-report or teledentistry	18 (32.8)
Ulcer
No	22 (40.0)
Yes	33 (60.0)
Taste alteration**
No	33 (60.0)
Yes	22 (40.0)
Candidiasis
No	40 (72.7)
Yes	15 (27.3)
Xerostomia
No	41 (74.5)
Yes	14 (25.5)
Periodontal diseases
No	51 (92.7)
Yes	4 (7.3)
Herpes Simplex
No	51 (92.7)
Yes	4 (7.3)

• *PCR: polymerase chain reaction
• **Taste alteration: anosmia. dysgeusia or ageusia

The PCR diagnostic test was the most used, present in 76.4% (n=42) of the articles. About half of the studies (43.6%, n=24), the oral manifestations were diagnosed by clinical examination (physician or dentist diagnosis). The oral manifestation most frequent was ulcer (60.0%, n=33), followed by taste alteration (n=22, 40.0%), and candidiasis described in 15 studies (27.3%) and xerostomia in 14 studies (25.5%). The described onset time of oral manifestations in the analyzed studies ranged from less than 21 days (before diagnosis of COVID-19) to 150 days after diagnosis of COVID-19.

Regarding the most prevalent lesion according to each type of study (Table 2), it was observed that ulcer lesion was the most reported in case report studies. In contrast, taste alteration was most present for analytical observational studies, followed by ulcer and xerostomia. When considering the type of examination, most studies that performed clinical and laboratory examinations were case reports and case series. Considering self-report and teledentistry, there was a slight preference for its use in analytical observational studies.

Table 2
Comparison analysis between the oral manifestations of lesions, their diagnoses, and the design of the studies (n=55).

	Case report	Case series	Cross-sectional	Cohort	Caso-Control
Ulcer
No	9 (40.9)	4 (18.2)	3 (13.6)	5 (22.7)	1 (4.6)
Yes	12 (36.4)	9 (27.3)	7 (21.2)	5 (15.1)	0 (0.0)
Taste alteration*
No	17 (51.5)	8 (24.2)	3 (9.1)	4 (12.1)	1 (3.1)
Yes	4 (18.2)	5 (22.7)	7 (31.8)	6 (27.3)	0 (0.0)
Candidiasis
No	18 (45.0)	8 (20.0)	8 (20.0)	5 (12.5)	1 (2.5)
Yes	3 (20.0)	5 (33.3)	2 (13.4)	5 (33.3)	0 (0.0)
Xerostomia
No	20 (48.8)	11 (26.8)	5 (12.2)	4 (9.8)	1 (2.4)
Yes	1 (7.1)	2 (14.3)	5 (35.7)	6 (42.9)	0 (0.0)
Periodontal disease
No	21 (41.2)	13 (25.5)	9 (17.6)	8 (15.7)	0 (0.0)
Yes	0 (0.0)	0 (0.0)	1 (25.0)	2 (50.0)	1 (25.0)
Herpes simplex
No	20 (39.3)	12 (23.6)	9 (17.6)	9 (17.6)	1 (1.9)
Yes	1 (25.0)	1 (25.0)	1 (25.0)	1 (25.0)	0 (0.0)
Diagnosis of oral manifestations
Clinical examination	11 (45.8)	5 (20.8)	3 (12.5)	4 (16.7)	1 (4.2)
Laboratory examination	6 (46.1)	5 (38.5)	0 (0.0)	2 (15.4)	0 (0.0)
Patient self-report or teledentistry	4 (22.2)	3 (16.7)	7 (38.9)	4 (22.2)	0 (0.0)

• *Taste alteration: anosmia, dysgeusia or ageusia.

Discussion

This was the first article to verify the influence of study design in the report of oral manifestations of COVID-19 related articles. We found that the reported oral manifestations are different depending on the study design, as well as there is a divergence and non-standardization of the diagnostic method performed in these studies. Moreover, there is no standardization in reporting the data evaluated, such as oral lesions.

Related to the oral lesions identified, ulcer was the most reported lesion in case reports and case series studies, agreeing with previous literature²²,⁶³. Furthermore, these studies presented a diagnosis of the oral manifestations through clinical examination. A possible explanation for this finding is that these lesions were more noticeable due to the direct damage to the oral tissue and mucosa, causing pain and discomfort, often requiring specialized care by patients⁸. In addition, some publications show that the edema⁴⁷ and ulcers were found in patients who required oxygen or intubation⁷ and it is unlikely that these oral lesions were a direct manifestation of the virus or a marker of the progression of COVID-19⁷. In this sense, the relationship between ulcers and COVID-19 should be interpreted with caution, as they may be biased by the study design and lack of theoretical causal plausibility.

In agreement with previous literature, the oral condition that appeared the most in the group of analytical observational studies was taste alteration¹³,¹⁴,²⁶,⁵¹, diagnosed by questionnaires and patient self-report⁵,⁶⁴,⁶⁵. There is still no consensus on the hypothesis and mechanism of action between COVID-19 and taste alteration; however, the data collection method of these studies can be discussed. Applying data collection by questionnaires and online format may make it easier to interpret oral symptoms, such as loss of taste, and have hindered the visual diagnosis of other oral lesions, thus making it challenging to interpret oral signs and symptoms during or after COVID-19⁶⁵. Moreover, one of the first reports of symptomatology in COVID-19 patients was taste alteration. This report may have had a nocebo effect on patients, being a consequence of previous reports from other patients about such a symptomatologic possibility and may have then caused interference when answering the questionnaire⁶⁶.

After analyzing the studies in this research, some oral lesions were reported in a smaller number, such as herpes simplex¹⁰,⁶⁷, oral lichen planus⁶⁸, mucormycosis⁴¹,⁴⁴, and osteonecrosis⁵⁸, among others⁴³. These manifestations may be considered opportunistic lesions with great potential to affect patients, often resulting from actions for the treatment of COVID-19 and the deterioration of systemic health⁹. Other authors also report that several factors can affect the oral mucosa and trigger numerous lesions, including lack of oral hygiene during the disease, stress, and secondary infections⁶⁸. In addition, these manifestations are some of the most common factors which can cause immune dysregulation in the oral cavity⁶⁸and be present in patients with COVID-19.

Most of the studies analyzed were case reports and case series, which critically agree with other reviews that mapped the level of evidence of published studies on COVID-19⁸. These studies have the lowest level of scientific evidence when considering the different pyramids of evidence⁶⁹ because they have several methodological biases, no comparison group, and low reproducibility. The fact that no clinical trials were found shows the scarcity of studies with high methodological levels within the theme and when discussing the level of evidence. However, because this is a pandemic period, with restrictive measures and no knowledge about the disease scenario, the large number of case report studies and case series becomes plausible. Moreover, cohort studies are a reliable design to determine the occurrence of the disease, identify risk factors, and even determine a causal relationship. In the present review, these studies were most of the analytical observational studies found. Being aware that the hierarchical scale of evidence is not linear⁷⁰ and when well conducted, a cohort study can be very reliable⁷¹.

An important aspect to consider in this study is that most of the studies performed the diagnosis of lesions through clinical examination by health professionals, but the use of criteria for diagnosis of lesions or training and calibration of examiners was not reported. The diagnosis of oral diseases has a high degree of subjectivity and depends of professional qualification, so the World Health Organization (WHO) recommends and reports that it is crucial to use the technical guide to calibrate oral disease examiners⁷². Furthermore, taking into consideration that the diagnostic method performed was basically visual/tactile in clinical examinations, the possibility of reproducibility and sensitivity become weak, and some diseases may also not be recognized by examiners, causing a lack of diagnoses or underestimated lesions in each population⁷³.

With the impact of the pandemic, a minimal understanding of the behavior of the virus was necessary and, in the face of the restrictive measures imposed to contain the advance of the disease, one of the ways to produce and conduct new research was through teledentistry and online surveys with self-report⁷⁴,⁷⁵. In the group of analytical observational studies that were analyzed, self-report and teledentistry were methods commonly used as diagnosis. However, according to previous literature, online surveys do not guarantee consistent validity of results because there are limitations such as sample characterization and data collection method used, which may influence the research results⁷⁴. In this sense, different results between analytical observational studies and case reports/series may be related to the conduct of the study design, sample selection bias, and the use of non-validated methods, which may cause response bias or affect specific groups of people assessed⁷⁵.

There are some limitations of this study that need to be emphasized. First, COVID-19 is still a new disease, and its manifestations, characteristics, and sequelae are still challenging for researchers. Next, the lack of standardization in the questionnaires used, and the classification and nature of the lesions may have reflected on the results of this research since it made it difficult to collect the data in a standardized manner. Moreover, the necessity of rapid responses about covid and its consequences to reduce its harms and damages may be contributed for the researchers neglect some methodological aspects or reduce its quality criteria. However, the revisors of this study were trained to avoid errors or lack of data from the studies found. Third, the language restriction for selecting articles was only in English, which may have provided the non-inclusion of studies written in other languages since the pandemic started in China. However, English is considered the universal language in science, and studies conducted in Asia were found in greater numbers in this review.

Future research on this topic is encouraged to better plan the design of their studies, including designed studies with careful sample selection, training, and calibration for data collection for the examination of oral manifestations, and standardizing the diagnostic methods of the evaluated diseases.

This study concluded that the oral lesions present in patients with COVID-19 are different according to the study design and that these differences may be related to the diagnostic method used and the way of data reporting.

Acknowledgements

FRO and RSO are funded in part by Meridional Foundation (Passo Fundo – Brazil). This study was conducted in a Graduate Program supported by CAPES, Brazil – Finance Code 001.

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Edited by

Editor: Dr. Altair A. Del Bel Cury

Publication Dates

• Publication in this collection
  02 Aug 2024
• Date of issue
  2024

History

• Received
  05 June 2023
• Accepted
  25 Oct 2023