Trends in Small Animal Reproduction: A Bibliometric Analysis of the Literature

Simple Summary Reproduction in small animals is an expanding research area, with focus on breeding improvement and clinical management of domestic carnivores. The aim of the present study was to conduct a bibliometric analysis of the literature of the last decade on small animal reproduction, to point out main sources, most prolific countries, and emerging and neglected topics. Results show that research in biotechnologies for assisted reproduction has a central and increasing role in this field. Diversity in author keywords was also pointed out and a consensus to better categorize research in this field is proposed to reduce this problem in the future. Abstract Small animal reproduction (SAR) is a main research field in veterinary medicine and bibliometric analyses are useful to investigate trends in specific research areas. The objective of the present study was to conduct a bibliometric analysis of the literature of the last decade on SAR. A search equation was created, and documents were retrieved from the Web of Science database. Documents were manually revised, categorized and R software version 4.1.2 with Bibliometrix R package version 3.1 and MS Excel were used to perform the analyses. The included documents (n = 1470) were mainly research articles (78%). The top countries for the number of documents and citations were Brazil, United States, Italy, Poland, and Korea. These also account for the most prolific authors and institutions. Analyses by author keywords, categories, and recent reviews of the literature suggest that research on the canine species is more abundant than research on the feline one and that reproductive biotechnologies are a main research focus. Some clinical topics are still considered niche or neglected themes (e.g., semen collection in tomcats, neonatology). However, heterogeneity and ambiguity in keywords and categories are undeniable. This study offers interesting insights, providing definitions for main keywords in the field of SAR.


Introduction
In the field of veterinary sciences, small animal reproduction is becoming more important given the increased interest in breeding of companion animals [1] and in studying domestic carnivores as a model to develop biotechnologies for endangered species conservation [2]. Nowadays many organizations promote specialization in the field of veterinary medicine all around the world (e.g., the American College of Theriogenologists-ACT, and the European College of Animal Reproduction-ECAR). These organizations are recognizing different subspecialties, among which also small animal reproduction. Continuing education in this field is promoted by societies such as the European Veterinary Society for Small Animal Reproduction (EVSSAR). Conferences and meetings are regularly organized, and academics and practitioners are encouraged to share their knowledge and experience In total, 2856 documents matching the search criteria were retrieved. On documents were deemed as pertinent to small animal reproduction. The annual ev of publications during this time span is reported in Figure 1. The annual grow was4.92%; however, the trend was not regular, with 2012 being the most prolific y 200) followed by 2020 (n = 165). The mean number of documents per year was 14 SD). Most of the retrieved publications were research articles (n = 1148, 78.1%), f by meeting abstracts (n = 215, 14.6%), reviews (n = 48, 3.3%), proceeding papers 2.5%), corrections (n = 12, 0.8%), and letters (n = 11, 0.7%).
The distribution of the retrieved documents by research areas according to reported in Table 1 and majority of publications were included in the subj "Veterinary Sciences" (n = 613, 41.7%). The canine species was more represented feline species (n = 937 and n = 479), although some papers focused on both (n = 54

Sources
The number of journals that published documents on small animal reproduct 288. Reproduction in Domestic Animals (n = 334, 22.7%) and Theriogenology (n = 164 The distribution of the retrieved documents by research areas according to WoS is reported in Table 1 and majority of publications were included in the subject area "Veterinary Sciences" (n = 613, 41.7%). The canine species was more represented than the feline species (n = 937 and n = 479), although some papers focused on both (n = 54).

Sources
The number of journals that published documents on small animal reproduction was 288. Reproduction in Domestic Animals (n = 334, 22.7%) and Theriogenology (n = 164, 11.2%) Animals 2022, 12, 336 4 of 16 were the most prolific journals as well as the most cited, as confirmed by the Bradford's Law plot, indicating these two journals as the core sources of the whole collection ( Figure 2). Table 2 reports the twenty most prolific journals with their 2020 impact factor and rank. These sources published 34% of the papers regarding small animal reproduction between 2012 and 2021.
Animals 2022, 12, x 4 were the most prolific journals as well as the most cited, as confirmed by the Bradf Law plot, indicating these two journals as the core sources of the whole collection (Fi 2). Table 2 reports the twenty most prolific journals with their 2020 impact factor and r These sources published 34% of the papers regarding small animal reproduction betw 2012 and 2021.

Authors and Affiliations Analysis
Authors involved in publications on small animal reproduction were 4874 in the last decade, with a mean of 3.32 authors per documents and 0.3 documents per author. Most of the documents were authored by more than one person (n = 1399, 95.2%), with only 71 single-authored documents (4.8%). Furthermore, 75% of the authors participated in just one publication (n = 3659), whereas 1040 authors appeared in two to five articles (21.4%) and only 175 authors (3.6%) participated in more than five publications. The co-authorship analysis, considering the ratio between the total number of authors of multi-authored papers and the total number of multi-authored papers, revealed a collaboration index of 3.44 and 5.53 co-authors per document.
Both academic and research institutes (n = 731) and private laboratories, veterinary clinics and hospitals (n = 325) contributed to the literature.
To analyze country contribution, the corresponding author's affiliation was considered.

Most Relevant Papers and Citation Analysis
The impact of publications in the field of small animal reproduction was assessed analyzing data from citation indexes. A total of 30,635 references were included in the 1470 retrieved documents, whit a mean number of 5.59 citations per document and a total of 5769 articles citing the ones included in the present bibliometric analysis. Papers that received more than 10 citations were 269, representing 18.3% of the total. Most of The twenty most cited papers are reported in Table 3, they account for 15% of the citations for this collection (n = 864) and they were published by 15 journals. The journals Theriogenology and Reproduction in Domestic Animals contributed, respectively, with six and four papers to the list of the most relevant documents (Table 3), accounting for 24.9% (n = 1440) and 20.6% (n = 1187) of the citations, respectively, for a total number of citations equal to 2627 (45.5%).

Analysis by Keywords
The total number of keywords chosen by authors for this collection was 2536, with dog (n = 327), canine (n = 131), cryopreservation (n = 86), uterus (n = 72), ovary (n = 67), feline (n = 61), testis (n = 54), reproduction (n = 47), sperm (n = 47), and semen (n = 42) being the  Figure 3. Keyword plus were also retrieved (n = 3268) as they are a WoS tool for capturing the content and scientific concepts presented in articles. In this case, spermatozoa (n = 120), dogs (n = 114), cryopreservation (n = 108), motility (n = 71), semen (n = 57), cat (n = 54), fertility (n = 51), artificial insemination (n = 50), oxidative stress (n = 50), and fertilization (n = 47) were the most frequent. When these keywords are grouped according to Medical Subject Headings (MeSH controlled vocabulary) the frequencies of appearance in the author's keywords changes slightly, as reported in Table 4.  Figure 4 shows the co-occurrence analysis of the most frequent author keywords. The size of the node is proportional to the frequency of the keyword, while the thickness of the line connecting two keywords represents the strength of the relationship. The four colors represent the different clusters revealed by the network analysis. When these keywords are grouped according to Medical Subject Headings (MeSH controlled vocabulary) the frequencies of appearance in the author's keywords changes slightly, as reported in Table 4. Figure 4 shows the co-occurrence analysis of the most frequent author keywords. The size of the node is proportional to the frequency of the keyword, while the thickness of the line connecting two keywords represents the strength of the relationship. The four colors represent the different clusters revealed by the network analysis.  A multifactorial analysis was also performed to see how the most frequent author keywords relate. Therefore, Figure 5 shows that the most used keywords in the field of small animal reproduction are grouped in just two main clusters. Nodes are close to each other when a large proportion of documents treat them together.  A multifactorial analysis was also performed to see how the most frequent author keywords relate. Therefore, Figure 5 shows that the most used keywords in the field of small animal reproduction are grouped in just two main clusters. Nodes are close to each other when a large proportion of documents treat them together. A multifactorial analysis was also performed to see how the most frequent author keywords relate. Therefore, Figure 5 shows that the most used keywords in the field of small animal reproduction are grouped in just two main clusters. Nodes are close to each other when a large proportion of documents treat them together. A thematic map was created by using a two-dimensional matrix considering centrality and density as measurements to highlight the most important topics in the field of small animal reproduction. Centrality measures the relevance of a topic, while density estimates the development of a theme. The upper right quadrant is occupied by important and well-developed themes, lower left emerging or declining themes, upper left well-developed themes, and lower right transversal basic themes. The clusters are represented by bubbles within the map, which are labeled by keywords with the highest occurrences, and A thematic map was created by using a two-dimensional matrix considering centrality and density as measurements to highlight the most important topics in the field of small   Finally, the sorting of documents into EVSSAR categories (Figure 7) show that "Biotechnologies for assisted reproduction in carnivores" and "Physiology and clinics of reproduction" are the main fields of recent research in small animal reproduction (40.2% and 22.2%, respectively). Finally, the sorting of documents into EVSSAR categories (Figure 7) show that "Biotechnologies for assisted reproduction in carnivores" and "Physiology and clinics of reproduction" are the main fields of recent research in small animal reproduction (40.2% and 22.2%, respectively). Figure 7. Distribution of documents included in the present study into EVSSAR (European Veterinary Society for Small Animal Reproduction) "selected papers" section (2020). *: "Biotechnologies for assisted reproduction" and "Physiology and clinics of reproduction" are the categories that include the highest percentage of documents.

Latest Reviews in the Field of Small Animal Reproduction
Literature reviews are the keystone of evidence-based medicine, and they are essential to select further research topics, to have an idea on the state-of-the-art in specific areas. The collection analyzed in the present study included 49 reviews. The review articles pub- Figure 7. Distribution of documents included in the present study into EVSSAR (European Veterinary Society for Small Animal Reproduction) "selected papers" section (2020). *: "Biotechnologies for assisted reproduction" and "Physiology and clinics of reproduction" are the categories that include the highest percentage of documents.

Latest Reviews in the Field of Small Animal Reproduction
Literature reviews are the keystone of evidence-based medicine, and they are essential to select further research topics, to have an idea on the state-of-the-art in specific areas. The collection analyzed in the present study included 49 reviews. The review articles published in the last 5 years on small animal reproduction (title, author, year, journal, subfield, author keywords) are reported in Table 5, to emphasize topics on which scientists recently decided to focus to address the need of summarizing scientific knowledge. Three main subfields were identified: biotechnologies, clinical sciences, and physiology. Eleven papers were assigned to the subfield "clinical sciences" (47.9%), nine papers to the subfield "biotechnologies" (39.1%), and three documents were included in the subfield "physiology" (13%).

Discussion
The present bibliometric analysis had the objective of exploring contributions, trends, impact, and dynamics in research on small animal reproduction. During the last decade, research in this field has decreased based on this analysis. At first sight, this may seem counter intuitive, but it must be noted that 2020 has so far been the second most prolific year ever in small animal reproduction research. If we evaluate the mean number of publications per year of the previous decade (2002)(2003)(2004)(2005)(2006)(2007)(2008)(2009)(2010)(2011), it is obvious that this number is lower than in the last decade (118.6 ± 39.5 and 147 ± 22.7, respectively), suggesting a generally increasing interest in research on small animal reproduction.
Main research areas according to WoS were 'Veterinary Sciences' and 'Reproductive Biology'. Although, journals in WoS can be assigned to multiple research areas and this can lead to ambiguous classification of papers into research areas. This could explain why many papers concerning canine semen were assigned to the research area 'Agricultural Dairy Animal Science'.
Most of the documents were research articles and the theme-oriented journals Reproduction in Domestic Animals and Theriogenology were the core sources of the collection. Brazil, USA, Italy, Poland, and Korea were the most productive countries, also showing the highest inter-country collaboration rate. These countries account for almost 50% of the total scientific research about small animal reproduction. Accordingly, the universities of Milan (Italy), Wroclaw (Poland), and São Paulo (Brazil) were the most prolific, also being the affiliations of the most cited authors in this collection.
Literature on the canine species doubles that in the feline species, although this is not surprising as it reflects the numbers of published papers on dogs and cats in general (154,535 in dogs versus 67,568 in cats, according to research on WoS). Furthermore, the trend lines show that research on canine reproduction is also increasing more than research on feline reproduction in terms of the number of published papers. However, the importance of the feline species as a topic of research in animal reproduction is increasing, especially in relation to the interest in studying cats to improve technologies for assisted reproduction (ARTs) in endangered wild felids. Most of the wild felids are considered at risk, and cats represent a good model to develop research in this area [50]. This is emphasized by the fact that the keywords "cat", "oocyte", "ovary", "vitrification", and "in vitro maturation" belong to the same cluster in our analysis, meaning that these keywords often appear together in recently published papers. Furthermore, they represent a very central theme in research. The interest in dogs as a research model for wild canids conservation is limited for two reasons: there are not many endangered species [50] and assisted reproductive biotechnologies such as in vitro fertilization (IVF) are at present no routine practice in dogs [2]. Nevertheless, the keywords "dog" and "canine" are clustered with terms belonging to the spheres of gynecology (uterus, pyometra), andrology (testis, testosterone, spermatogenesis), with many appearances also in the area of male biotechnologies (cryopreservation, sperm, epididymis, CASA-Computer Assisted Sperm Analysis, sperm quality, semen). This is not surprising given the high interest in the use and conservation of dog semen. The interest lies especially in maximizing the profit of breeders and, most of all, of in improving the availability of genetic material to guarantee diversity [51]. The recurrence of the keywords indicating the feline species is lower in this area. However, research on biotechnologies in tomcats is very actual and was targeted by multiple reviews of the literature, underlining the interest of researchers for the topic [28,43,44], even if it still considered as a niche subject. In general, reproductive biotechnologies represent an important area of research in small animal reproduction, surpassing research on clinical aspects of reproduction by a factor of two. This could be associated with the practical and ethical limitations in conducting clinical research compared to the fast collection and processing of samples in the field of biotechnologies [52], along with the already cited interests in applying assisted reproductive technologies to other species and increasing breeding performances. The present study also shows how some themes are considered the core of small animal reproduction, with topics such as uterine pathologies, pyometra in the bitch, and canine semen being the focus of extensive research in the last decade. On the other hand, literature on neonatology (i.e., studies regarding puppies and kittens from birth to weaning) in general seems to be lacking and topics such as neonatal mortality are considered niche themes. However, neonatology and pediatrics represent everyday interests for veterinarians, breeders, and pet owners and neonatal mortality is still considered a main issue in domestic carnivores [53,54].
A huge heterogeneity in keywords used by the authors was noticed, with the most reported word ("dog"), being chosen only 314 times, and double if we also considered the MeSH terms. However, not all databases are using controlled vocabulary and therefore, working on a consensus on keywords use should be encouraged. This is the reason why we chose to perform a further analysis of the included documents by sorting them into EVSSAR "selected papers" categories. The sorting was manually performed, but many documents could be sorted into more than one category. For example, many articles about semen could be classified as "Biotechnology for assisted reproduction, Spermatozoa", and even "Andrology". Additionally, articles about artificial insemination could be categorized both as "Physiology and clinics of reproduction" and "Biotechnologies for assisted reproduction".
Hereafter we propose keywords based on EVSSAR "selected papers" categories. These keywords should be used in research on small animal reproduction to classify papers into main topics. Definitions are also provided.
Physiology of reproduction: Research on the function of healthy reproductive organs, tissues, cells, molecules, and chemical processes concerning small animal reproduction.
Gynecology: Any clinical practice dealing with the female reproductive system of small animals, including diseases of the female reproductive organs and mammary glands, endocrinological changes of the normal cycle, breeding soundness evaluation and infertility, determination of the phase of the cycle, and any pathology of pregnancy, parturition and post-partum period.
Andrology: Any clinical practice dealing with the male reproductive system of small animals, including diseases of the male reproductive organs, endocrinological deviations, breeding soundness evaluation and infertility, semen analysis with no intervention or modification on the semen by the operator after collection.
Biotechnology for assisted reproduction: Technologies applied to germ cells, gametes, and embryos with an effect of small animal reproduction. This includes practice and research on techniques including artificial insemination, embryo transfer, in vitro maturation, in vitro fertilization, in vitro production, intracytoplasmic sperm-injection, cryopreservation of sperm, oocytes and embryos, sperm and embryo sexing, cloning, nucleus transfer, and gene transfer.
Contraception: Artificial (medical or surgical) techniques aimed to prevent pregnancy in small animals.
Neonatology: Treatment and care of newborn kittens and puppies from birth to weaning. The most cited documents of this bibliometric analysis belong to the field of small animal reproduction, but some of them represent crossroads with fields such as Infectious Diseases, Behavior, Anesthesiology, and Pathology. In fact, the paper with the highest number of citations is "Coxiella burnetiid associated reproductive disorders in domestic animals-a critical review" by [7]. This paper focuses on domestic animals in general and the canine and feline species only have a marginal role in it. Nevertheless, Coxiella burnetii is an intracellular bacterium causing Q fever in humans and reproductive disorders in mammals. Periparturient cats have been implicated in several outbreaks of Q fever in humans; therefore, the importance of this topic is undeniable, and the focus on public health justify the high number of citations. However, all the other relevant papers focus on the canine and feline species, deepening the fields of Clinical Sciences, Physiology, and Biotechnology.
It needs to be mentioned that the results for the research equations included a great number of papers on canine and feline mammary tumors, representing more than 40% of the whole collection. Papers were checked by the authors and only the ones deemed as pertinent to small animal reproduction were included in the analysis. Specifically, papers focusing on the association between mammary tumors and the presence of sexual steroids, on the effect of spaying on mammary neoplasms, on the co-occurrence with other reproductive pathologies, and papers clinically and surgically oriented were included, whereas articles strictly related to pathology, histology, immunohistochemistry, and chemotherapy were excluded. Research on mammary tumors in small animals is extensive, not only for the high incidence of mammary neoplasms in domestic carnivores [55,56], but also for the role of the canine and feline species as a model for human breast cancer [57,58]. This explains the high degree of development of this research area, and the decision to select only papers fitting the field of small animal reproduction was mandatory in order to avoid a huge bias in results. Additionally, the revision of the included papers helped in avoiding the biases deriving from the sole use of tools such as Bibliometrix and WoS. A possible limitation of the present study is that the research was conducted solely in WoS [59] in a limited time frame (2012-2021), leading to the exclusion of papers and sources not included in WoS or published before 2012, with possible underestimation of the comprehensive literature.

Conclusions
The present study is the first bibliometric analysis in the field of small animal reproduction, offering interesting insights about research evolution and development, pointing out what topics are considered basic knowledge in this area, with consolidated data and extensive research, what research areas are currently neglected, and what are the emerging topics that scientists are currently investigating, such as canine and feline biotechnologies. Furthermore, we provide definitions for keywords to be used for papers and database searches in the field of small animal reproduction with the aim of adding homogeneity to this complex and wide field of research.