The use of H-index to assess research priorities in poultry diseases Kateri Bertran,*,y,1 Martí Cortey,z and Ivan Díaz*,y *IRTA, Centre de Recerca en Sanitat Animal (CReSA, IRTA-UAB), Campus de la Universitat Aut onoma de Barcelona, Barcelona, 08193 Bellaterra, Spain; yOffice International des Epizooties (OIE) Collaborating Centre for the Research and Control of Emerging and Re-emerging Swine Diseases in Europe (IRTA-CReSA), Bellaterra, Barcelona Spain; and zDepartament de Sanitat i Anatomia Animals, Universitat Aut onoma de Barcelona (UAB), Barcelona, 08193 Bellaterra, Spain ABSTRACT Identifying which diseases represent a practices and management throughout history. Thus, priority is crucial to optimize resources for diagnostics, Others were the most cited pathogens until the 1970s control, and prevention. Here, the impact of 111 and, following 3 decades of unpopularity because of poultry pathogens belonging to Viruses (n 5 31), widespread use of intensive production practices, Bacteria (n 5 33), and Other (n 5 47) was assessed regained importance in the 2000s thanks to welfare using the H-index. The overall mean H-indexes sug- regulation changes. Citations for Bacteria increased gested that poultry Viruses have statistically greater especially from the 1990s onward, probably because of impact than Bacteria, which in turn are statistically the ban of growth promoters in western countries and more relevant than Others. Among the 20 highest the need to find new control methods for bacterial and H-indexes, 45% were zoonotic, and almost a third was protozoal infections. In general, countries with the Office International des Epizooties-listed. Avian influ- greatest poultry production and research budgets had enza virus (H-index 127), Salmonella enteritidis and higher research production, that is the United States of Salmonella typhimurium (H-index 72), and Eimeria America (USA) and China. Interestingly, the United spp (H-index 70) ranked the highest in Virus, Bacteria, Kingdom was among the top research producers and Other, respectively. Pathogens that produce overt despite falling behind other countries in poultry pro- clinical diseases and economic damage, cause immu- duction and research budget. Moreover, the USA nosuppression, and/or are zoonotic had the highest exhibited the strongest poultry research production H-index scores. The evolution of citations of particular based on number and diversity of publications pathogens reflected severe poultry outbreaks and/or (Dcos-index). In conclusion, the H-index could be a zoonotic outbreaks in relatively wide geographic areas. valid, simple tool to prioritize funding or interest in Also, the evolution of citations based on taxonomic poultry diseases, especially when used as a preliminary groups mirrored major changes in poultry production selection approach in combination with other metrics. Key words: poultry, pathogen, H-index 2020 Poultry Science 99:6503–6512 https://doi.org/10.1016/j.psj.2020.09.017 INTRODUCTION Ritchie and Roser, 2019). Infectious diseases of poultry not only threaten the poultry industry worldwide but Global production of poultry meat has increased can also affect public health and wildlife conservation. rapidly over the past 50 yr and is currently the world’s As a result, diseases of poultry have consequences that primary source of animal protein, with growing trends go beyond losses on farms and include poultry trade pro- all over the world (Shahbandeh, 2018; FAO, 2019; hibition, food insecurity in developing countries, and risk of fatal human infections. The poultry industry worldwide is strikingly diverse Ó 2020 The Authors. Published by Elsevier Inc. on behalf of Poultry and complex in the type of farms and the range of species Science Association Inc. This is an open access article under the CC BY- bred. On the one hand, farms vary from large industrial- NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/). ized integrated production systems to small extensive, Received August 17, 2020. Accepted September 4, 2020. rural, family based systems supporting livelihoods and 1 Corresponding author: kateri.bertran@irta.cat supplying local or niche markets (FAO, 2019). On the 6503 6504 BERTRAN ET AL. other hand, chickens, turkeys, ducks, and geese are the Table 1. Distribution of pathogens of the major poultry production primary source of eggs, meat, and/or feathers, but other species used in the study. species such as guinea fowl, quail, pheasants, partridges, Zoonotic and ostriches also contribute, albeit in a smaller scale, to Total potential OIE-listed 2 agricultural production and livelihoods in both devel- Taxonomic group Number % Number % Number % oped and developing countries (Sims et al., 2016). To Virus 31 28 4 13 9 29 complicate things further, some species or even breeds Bacteria 33 30 18 55 5 15 are more abundant in certain continents, countries, or Other1 47 42 18 38 0 0 production systems (Sims et al., 2016; FAO, 2019). Total 111 40 36 14 13 This intricate scenario hampers effective detection and 1 Other includes helminths, protozoa, external parasites, fungi, and control strategies designed to fight against infectious mycotoxicosis. 2 OIE list of 2020 (OIE, 2020). diseases. The economic impact of diseases is difficult to assess, especially in a production system in which the economic fungi (plus mycotoxins) were included. The final data- return is based not only on flock productivity but also on base (Table 1) comprises the distribution of pathogens product quality and viability (Collett, 2020). To effec- based on the aforementioned taxonomic division, their tively target and optimally use disease diagnostics, con- zoonotic potential, and whether they cause an Office In- trol, surveillance, and prevention efforts, as well as ternational des Epizooties (OIE)-notifiable disease as of funding priorities, it is crucial to identify which diseases 2020 (OIE, 2020). The major internationally recognized are a priority in poultry. The H-index was initially pro- reference book in poultry veterinary medicine “Diseases posed as a measure of a researcher’s scientific output of poultry” (Swayne et al., 2020b) was the main source based on counting the number of publications (N) by to construct the final database of pathogens. Other sour- that researcher cited N or more times (Hirsch, 2005). ces such as International Committee on Taxonomy of This metrics shortly became relevant across most fields Viruses (https://talk.ictvonline.org/), The Poultry of science (Kustritz and Nault, 2019) and is nowadays Site (https://thepoultrysite.com/publications/diseases- displayed in the researcher profiles on citation databases of-poultry), FAO (http://www.fao.org/home/en/), such as Scopus, Web of Science (WOS), and Google and NCBI Taxonomy (National Center for Scholar. Regrettably, the H-index has also become a Biotechnology Information: Taxonomy browser, 2020) “magic tool” to summarize the science quality of a candi- were also used to complete the list of pathogens. date’s career in the hands of hiring committees and fund- ing agencies (Kreiner, 2016). Despite its criticisms (Gasparyan et al., 2018; Conroy, 2020; Hirsch, 2020) Calculation of the H-index Scores and and a growing number of alternative indexes attempting Comparison With Other Indexes to overcome its limitations (Wildgaard et al., 2014), the H-index is still the most popular bibliometric index The bibliographic software package WOS (www. worldwide. Noteworthy, this metric seems to be a good webofknowledge.com) was used to calculate H-index quantitative indicator of disease impact both in humans scores. Searches were undertaken during March and (McIntyre et al., 2011; Cox et al., 2016; Sweileh, 2017) April 2020 and were restricted to publications in English and in domestic animals (McIntyre et al., 2014; Diaz between years 1900 and 2019, both inclusive. Similar to et al., 2016; Murray et al., 2016). Díaz et al. (2016), multiple names, synonyms, and acro- The main objective of the present work was to analyze nyms used over time for a given pathogen, and even the the relevance and impact of avian pathogens in the ma- name of the lesions or the disease caused by a given path- jor poultry production species using the H-index. The ogen, were used in the searches (Diaz et al., 2016). Terms evolution and geographical distribution of the publica- as “poultry”, “chicken”, “hen”, “rooster”, “broiler”, “fowl”, tions contained in the H-indexes cores (defined as the “turkey”, “duck”, and “goose” were used to delimit the publications included in the H-index) were also exam- searches to avoid including studies in species other ined and compared with the census of the poultry species than the ones evaluated here. The Boolean options and the research budgets per country. “AND” and “OR”, and “NOT” for exclusion terms were used when necessary to link multiple search terms. When searching, several biases occurred (Diaz et al., MATERIALS AND METHODS 2016); consequently, publications in the automatically Selection of Pathogens generated lists were curated one by one to ensure data- base accuracy. Publications related to poultry products The study comprises known organisms (from now on, or wild animals were not considered. The total number pathogens) that cause infection/infestation in the major of citations for the publications included in the H-index poultry production species which are chickens, turkeys, cores were calculated over time from each taxonomic ducks, and geese. The H-index was calculated for a total category as well as from the 20 highest H-index scores of 111 pathogens: Viruses (n 5 31), Bacteria (n 5 33), regardless of the taxonomy. In the latter, the percentage and Other (n 5 47); in Other, helminths, protozoa, of yearly increase of citations from the first publication of external parasites (classes Insecta and Arachnida), and the 20 highest H-index scores was also noted. H-INDEX IN POULTRY DISEASES 6505 The ranking generated by the H-index scores was 150 compared with the prioritization of pathogens obtained a b c using other indicators. Because there were noticeable dif- ferences among pathogens regarding year of the first 120 description or year of the first publication included in the H-index core, the M-quotient (Hirsch, 2005) (i.e., H-index score divided by years from oldest publication included in the H-index core) was calculated. The A-in- 90 H-index dex (Jin et al., 2007) (i.e., mean number of citations of publications that are included in the H-index core) was directly obtained from the WOS output. 60 Origin of the Research Productivity 30 The total number of citations, the mean citations per publication, and the country of origin of the publications were directly obtained from the WOS output. Three- letter country codes defined by the International Organi- 0 zation for Standardization (ISO-3166-1) (ISO: Online Virus Bacteria Other Browsing Platform, 2020) were used. To accurately assess the impact of each country’s research, the Dcos Figure 1. Box plot. Box plot of the H-index score quartiles for the ma- (Deciphering Citations Organized by Subject)-index, jor poultry production species according to taxonomic groups Virus, consisting of 2 figures (i.e., number of publications that Bacteria, and Other for the 1900–2019 period. Other includes helminths, a certain individual, institute, or country holds within protozoa, external parasites, fungi, and mycotoxicosis. (1) Mean. Let- ters show significant differences a . b . c (P , 0.05). the set of publications included in the H-index core of a given area or subject, plus the number of different areas with publications in the H-index cores) was also calculated (Diaz et al., 2016). In addition, the total num- found. When such grouping was done within each taxo- ber of publications included in the H-index cores was nomic group, significant differences were observed for summarized by continents. The 2018 census of chickens, OIE-listed status in Bacteria (OIE-listed turkeys, ducks, and geese per country was obtained from 35.6 6 8.0 . not OIE-listed 21.8 6 17.7) and for zoo- FAOSTAT (http://www.fao.org/faostat/). The most notic potential in Other (zoonotic 17.9 6 14.0 . not zoo- recent research and development (R&D) investment notic 12.0 6 14.0) (P , 0.05). by country was obtained from UNESCO (https://en. The highest frequency of H-index scores was observed unesco.org/), the World Bank (https://www. in the H-index interval 21–30 for Virus, in the interval worldbank.org/), and EUROSTAT (https://ec.europa. 11–20 for Bacteria, and in scores ,10 for Other eu/eurostat). (Figure 2). Of the 111 pathogens analyzed, almost 90% had an H-index ,50; only 10 pathogens had an H-index .50 (6 from Virus, 3 from Bacteria, and 1 from Other) Statistical Analyses and just 2 pathogens, which belonged to Virus, had an Microsoft Excel Software 2016 was used to calculate H-index .90. descriptive statistics. Box-plot representations and infer- Among the 20 highest H-index scores, 11 pathogens ential statistics were done using StatsDirect v3.2.8, were from Virus, 5 from Bacteria, and 4 from Other including nonparametric tests to compare H-index means (Table 2). Within each taxonomy group, avian influenza among taxonomic groups (Kruskal-Wallis test), zoonotic virus (H-index 127), Salmonella enteritidis and Salmo- potential, or OIE-listed status (Mann-Whitney test). A nella typhimurium (as etiological agents of salmonellosis) P-value of ,0.05 was considered to be significant. (H-index 72), and Eimeria spp (H-index 70) ranked the highest in Virus, Bacteria, and Other, respectively. Among the 20 highest H-index scores, 45% were zoo- RESULTS notic, 30% were OIE-listed, 10% were both zoonotic and OIE-listed, and 35% were in neither zoonotic nor H-Index Scores OIE-listed (Table 2). H-index scores were significantly different among all 3 taxonomic groups (means 6 SD): Viruses Comparison With Other Indexes 39.0 6 28.6 . Bacteria 23.9 6 17.2 . Other 14.4 6 14.2; (P , 0.05) (Figure 1). When pathogens The H-index and A-index rankings were similar were grouped by their zoonotic potential (zoonotic 25.5 (Table 3), given that number of citations of the publica- 6 24.7; not zoonotic 23.0 6 20.6) or by their tions in the H-index core tended to yield higher H-index OIE-listed status (OIE-listed 47.0 6 31.4; not OIE- scores especially for the highest H-index scores (Table 2). listed 20.6 6 18.4), significant differences were not In contrast, the H-index and M-quotient rankings 6506 BERTRAN ET AL. 40 (2010–2019), most citations belonged to Bacteria and 35 Others (Figure 4). 30 Number of pathogens 25 Research Productivity by Countries and 20 Continents 15 In most of the 20 highest H-indexes (15/20 patho- 10 gens), the United States of America (USA) was the first contributor of publications, in 1 case (avian leukosis vi- 5 rus) reaching a contribution of 84% (Table 2). In most 0 of the pathogens in which USA was not the first contrib- <10 11-20 21-30 31-40 41-50 51-60 61-70 71-80 81-90 91-100 >100 utor (4/5), this country held the second place. In general, H-index only 3 countries accounted for 50% of the publications of a given H-index core, with the exception of avian Figure 2. Frequency histogram. Frequency of the H-index scores ac- adenovirus 1 (Table 2). cording to taxonomic groups Virus (blue), Bacteria (green), and Other (brown). Other includes helminths, protozoa, external parasites, fungi, Europe had 40.7% of all publications (1,295 of 3,184 and mycotoxins. publications), followed by North America (35.1%), Asia (14.5%), Oceania (4.0%), Africa (3.6%), and South differed substantially, especially for the top 10 patho- America (2.2%) (Figure 5). Contributions from each gens, because years from oldest publication included in continent to a particular taxonomic group were overall H-index cores varied greatly among pathogens similar to the global contribution for that continent, (Table 3). A striking example of such disparity was with some exceptions. Thus, compared with their global Eimeria spp which, despite ranking eighth in H-index, percentages, North America and Asia contributed is ranked 18th in M-quotient because it held the oldest greater to Virus (39 and 20.1% of all Virus publications, publication (from 1929) in its H-index core. The opposite respectively), Europe and Oceania to Bacteria (44 and case was represented by avian influenza virus, which first 7.9%, respectively), and Africa and South America to publication in its H-index core was relatively recent Other (9.7 and 5%, respectively) (Figure 5). (from 1983), yielding both the highest H-index and the The USA, United Kingdom (UK, or GBR as per ISO highest M-quotient (Table 3). code, as shown in tables), and China were the greatest contributing countries in total publications (Table 4). These countries also topped the ranking when taxonomic Evolution of Citations groups were analyzed separately, except for Bacteria, for which the third contributor was Australia, and Other, The evolution of citations for the publications for which the third contributor was Denmark. The included in the top 20 H-index cores showed marked dif- USA accounted for almost one-third of the total publica- ferences among pathogens (Figure 3). Overall, a clear in- tions (32.5%), being the first contributor in all taxo- crease in number of citations was observed for all nomic groups. The second country with the highest pathogens from the 1980s onward, except for avian contribution overall and in each taxonomy was the UK leukosis virus, which increase was evident since the (11.4%). The third position was for China, which highest 1960s. In some cases, a steady increase in number of cita- contribution was for Virus, well beyond Bacteria and tions was followed by an abrupt growth for a short Other. Interestingly, when countries beyond the 10 high- period, such as avian influenza virus (2002–2009). For est total contributors were ranked for a specific taxo- other pathogens, such as avian leukosis virus, infectious nomic group, new countries appeared in the top 10; bursal disease virus, duck hepatitis B virus, or avian Ireland ranked 10th for Virus, Belgium fifth for Bacteria, pneumovirus, a constant increase was observed over whereas Brazil, Sweden, Austria, and Tanzania ranked time, but maximum number of citations was reached sixth, eighth, ninth, and 10th for Other, respectively several years ago, regardless of the year of the first pub- (data not shown). In contrast, some countries from the lication. Regarding avian leukosis virus, although its H- global top 10 ranked lower in specific taxonomic groups; index ranked second, the mean of percentage of yearly Denmark ranked 40th for Virus, the Netherlands ranked increase of citations from the first publication was one 11th for Bacteria, and China, Japan, and the of the lowest (1.3%). In contrast, the highest means of Netherlands ranked 18th for Other (Table 4). Based on percentage of yearly increase were seen for avian influ- Dcos-index, the USA was not only the major contributor enza virus (2.6%) and avian pneumovirus (2.4%). but also its research was evenly distributed among Up until the 1970s, Others were the pathogens mostly groups: 1,035 out of 3,184 total publications studying cited in the H-index cores (Figure 4). In the subsequent 91 out of 111 pathogens (Table 4). Similar results were 3 decades, citations for Viruses became predominant, obtained for this country when Dcos-index was calcu- whereas citations for Bacteria increased especially in lated for each taxonomic group. the 1990s and 2000s. Interestingly, Others regained Regarding poultry census, China topped chicken, popularity during the 2000s. During the last decade duck, and goose productions, whereas the USA was by H-INDEX IN POULTRY DISEASES 6507 Table 2. Pathogens of the major poultry production species with the highest H-index scores. Rank1 Pathogen Group2 H-index Zoonotic OIE-listed3 Total4 Mean 6 SD4 Countries5 1 Avian influenza virus Virus 127 X X 33,404 263.0 6 293.1 USA (36%), CHN (15%), GBR (8%) 2 Avian leukosis virus Virus 96 24,820 258.5 6 228.1 USA (84%), CHE (5%), GBR (3%) 3 Avian paramyxovirus (Newcastle) Virus 77 X X 10,967 142.4 6 82.7 USA (26%), GBR (16%), NLD (9%) 4 Infectious bursal disease virus Virus 76 X 9,148 120.4 6 48.0 USA (26%), DEU (17%), GBR (10%) 5 Infectious bronchitis virus Virus 73 X 8,259 113.1 6 45.6 GBR (42%), USA (22%), NLD (12%) 6 Duck hepatitis B virus Virus 72 9,683 134.5 6 75.3 USA (47%), DEU (17%), JPN (8%) 6 S. enteritidis, S. typhimurium6 Bacteria 72 X 7,869 109.3 6 37.7 GBR (36%), USA (32%), BEL (7%) 8 Eimeria spp Other 70 8,389 119.8 6 58.7 USA (39%), GBR (17%), CAN (7%) 9 Clostridium perfringens Bacteria 64 X 6,689 104.5 6 50.0 CAN (26%), USA (21%), BEL (10%) 10 Escherichia coli Bacteria 58 X 6,147 106.0 6 65.9 USA (24%), CAN (21%), ESP (8%) 11 Chicken anemia virus Virus 53 4,286 80.1 6 38.2 JPN (24%), IRL (24%), NLD (16%) 12 Avian adenovirus 1 Virus 51 3,703 72.6 6 30.7 USA (14%), DEU (12%), GBR (10%) 13 Reticuloendotheliosis virus Virus 49 4,127 84.2 6 43.5 USA (75%), JPN (4%)7 14 Mycoplasma gallisepticum Bacteria 48 X 3,357 70.0 6 24.7 USA (47%), AUS (15%), ISR (11%) 15 Avian reovirus Virus 44 2,950 67.1 6 23.6 USA (31%), ESP (22%), THA (13%) 16 Aflatoxins8 Other 43 X 3,448 80.2 6 38.6 USA (52%), TUR (11%), ARG (9%) 17 Pasteurella multocida Bacteria 42 X 2,861 68.1 6 57.5 USA (44%), AUS (38%), CAN (5%) 18 Avian pneumovirus Virus 41 X 2,757 67.2 6 23.5 GBR (57%), USA (24%), FRA (9%) 19 Fusarium spp Other 40 X 3,056 70.4 6 65.8 USA (40%), AUT (14%), CAN (10%) 19 Ochratoxins9 Other 40 X 2,999 75.0 6 34.8 USA (34%), IND (10%), DEU (6%) 1 Rank according to the H-index. 2 Other includes helminths, protozoa, external parasites, fungi, and mycotoxicosis. 3 OIE list of 2020 (OIE, 2020). 4 Total number of citations and mean number of citations 6 SD of the publications included in the H-index core. 5 Top 3 countries of origin of publications in the H-index core, and percentage of publications originating from the country. Three-letter country codes were used (International Organization for Standardization (ISO): Online Browsing Platform, 2020). GBR is used for the UK, United Kingdom of Great Britain and Northern Ireland (England, Scotland, Wales, and Northern Ireland). 6 Salmonellosis caused only by Salmonella enterica serovar Enteritidis and Salmonella enterica serovar Typhimurium were grouped together as the etiological agents of salmonellosis and separated from other Salmonella species and subspecies causing pullorum disease or fowl typhoid. 7 CZE, AUS, CAN, GBR, DEU, FRA, ISR, CHN, and CHE ranked third in contribution (2%). 8 Aflatoxins produced by Aspergillus flavus, Aspergillus parasiticus, and Penicillium puberulum. 9 Ochratoxins produced by Penicillium viridicatum and Aspergillus ochraceus. far the highest turkey producer (Supplementary development, such as certain adenoviruses, lymphoid Material S1). These 2 countries also had the largest leukosis virus, or avian paramyxovirus serotypes 2 to R&D budgets (Supplementary Material S2). In contrast 13, were excluded. Similarly, food-borne pathogens to the H-index scores, a variety of countries followed in generally considered commensals in birds, such as the ranking of top 10 poultry producers and R&D Campylobacter jejuni and C. coli (as opposed to spotty investment. liver disease-causing Campylobacter hepaticus), were not considered. Likewise, antimicrobial-resistant bacte- DISCUSSION ria studies were omitted. Besides, many pathogens have been renamed and taxonomically reclassified, Since Hirsch proposed it in 2005 (Hirsch, 2005), the H- hampering the distinction between renamed pathogens index has been both glorified and vilified (Gasparyan (e.g., Riemerella anatipestifer, previously Pasteurella et al., 2018; Conroy, 2020; Hirsch, 2020). Nonetheless, anatipestifer, Moraxella anatipestifer, and Pfeifferella the H-index has shown to be a valid alternative proxy anatipestifer) and emerging ones (such as Chlamydia for pathogen impact (McIntyre et al., 2011, 2014; Cox gallinacea). Searches were based on pathogens, not dis- et al., 2016; Diaz et al., 2016; Murray et al., 2016; eases; therefore, multipathogen syndromes, such as Sweileh, 2017). Furthermore, some limitations of the runting-stunting syndrome or poult enteritis mortality H-index occur to a lesser degree when applied to patho- syndrome, both caused by a myriad of viruses, were gens (reviewed by [Diaz et al., 2016]). In addition, not taken into account. measuring economic loss, prevalence, or mortality for The overall mean H-index scores suggested that pathogen risk prioritization appears highly time- poultry Viruses have statistically greater impact than consuming and not always comprehensive as opposed Bacteria, which in turn are statistically more relevant to measuring the H-index. Here, the impact of 111 path- than Others. Similarly, Diaz et al. (2016) found in ogens of the major poultry species (chickens, turkeys, swine that both Bacteria and Viruses were statistically ducks, and geese) was assessed using the H-index. more important than Others (Diaz et al., 2016). Some Only pathogens that cause a significant impact (i.e., well-known poultry viral diseases, such as avian influ- economic loss, prevalence, and/or mortality) in the enza, Newcastle disease, or infectious bronchitis, cause poultry industry were considered. However, it is worth economic damage by producing overt clinical diseases. mentioning that some difficulties encountered during However, many viruses reduce flock performance, and the searching process forced us to make certain decisions. thus economic profits, without appearing as overt clin- Thus, pathogens used only in cell lines or vaccine ical diseases. Some of their outcomes include stunting, 6508 BERTRAN ET AL. Table 3. Comparison of the 20 highest H-index scores with other bibliometric indicators. Pathogen Group1 Year2 H-index (rank) A-index3 (rank) M-quotient4 (rank) Avian influenza virus Virus 1983 127 (1) 263.02 (1) 3.43 (1) Avian leukosis virus Virus 1941 96 (2) 258.54 (2) 1.22 (6) Avian paramyxovirus (Newcastle) Virus 1946 77 (3) 142.43 (3) 1.04 (9) Infectious bursal disease virus Virus 1964 76 (4) 120.37 (5) 1.36 (5) Infectious bronchitis virus Virus 1967 73 (5) 113.14 (7) 1.4 (4) Duck hepatitis B virus Virus 1970 72 (6) 134.49 (4) 1.44 (3) S. enteritidis, S. typhimurium5 Bacteria 1975 72 (6) 109.29 (8) 1.60 (2) Eimeria spp Other 1929 70 (8) 119.84 (6) 0.77 (18) Clostridium perfringens Bacteria 1961 64 (9) 104.52 (10) 1.08 (8) Escherichia coli Bacteria 1956 58 (10) 105.98 (9) 0.9 (13) Chicken anemia virus Virus 1973 53 (11) 80.87 (12) 1.13 (7) Avian adenovirus 1 Virus 1957 51 (12) 72.61 (16) 0.81 (16) Reticuloendotheliosis virus Virus 1966 49 (13) 84.22 (11) 0.91 (12) Mycoplasma gallisepticum Bacteria 1952 48 (14) 69.94 (17) 0.7 (20) Avian reovirus Virus 1972 44 (15) 67.05 (20) 0.92 (11) Aflatoxins6 Other 1970 43 (16) 80.19 (13) 0.86 (14) Pasteurella multocida Bacteria 1962 42 (17) 68.12 (18) 0.72 (19) Avian pneumovirus Virus 1979 41 (18) 67.24 (19) 1.00 (10) Fusarium spp Other 1972 40 (19) 76.4 (14) 0.8 (17) Ochratoxins7 Other 1973 40 (19) 74.98 (15) 0.85 (15) 1 Other includes helminths, protozoa, external parasites, fungi, and mycotoxicosis. 2 Year: year of the oldest publication included in H-index cores. 3 A-index: mean number of citations of publications in the H-index core (Jin et al, 2007). 4 M-quotient: H-index/years from oldest publication included in H-index core (Hirsch, 2005). 5 Salmonellosis caused only by Salmonella enterica serovar Enteritidis and Salmonella enterica serovar Typhimurium were grouped together as the etiological agents of salmonellosis and separated from other Salmonella species and subspecies causing pullorum disease or fowl typhoid. 6 Aflatoxins produced by Aspergillus flavus, Aspergillus parasiticus, and Penicillium puberulum. 7 Ochratoxins produced by Penicillium viridicatum and Aspergillus ochraceus. malabsorption, and immune suppression, the latter field. This is in contrast to Bacteria, which prevention with insidious effects. In addition, owing to their and control using antimicrobials is relatively straight- frequent subclinical and multipathogen syndrome na- forward. Altogether, more resources have been devoted ture, the accurate diagnosis of viral infections can be to viral diseases in poultry than to any other etiolog- complex, allowing these pathogens to easily spread ical agent. and hindering their control. Moreover, efficacious vac- While a broader scientific interest would be ex- cines are not available for all viruses, and their effec- pected from a zoonotic and/or OIE-listed pathogen, tiveness is not immediate and easy to assess in the these categories did not necessarily increase the H- 130 AIV (2.6%) 120 ALV (1.3%) APMV-1 (1.4%) 110 IBDV (1.8%) 100 IBV (1.9%) 90 DHBV (2.0%) Salm (2.2%) 80 Eim (1.1%) Citations 70 Cl p (1.7%) E coli (1.6%) 60 CAV (2.1%) 50 ADV-1 (1.6%) 40 REV (1.8%) M gall (1.5%) 30 ARV (2.0%) 20 Afl (2.0%) 10 Pm (1.7%) APV (2.4%) 0 Fus (2.1%) Och (1.1%) Figure 3. Evolution of citations for the publications included in the H-index cores. Evolution of citations (from 1959 to 2019) for the publications included in the H-index cores of the 20 highest H-index scores and percentage of yearly increase of citations from the first publication. Lines (Virus); Dashed lines (Bacteria); Dotted lines (Other). Abbreviations: AIV, avian influenza virus; ALV, avian leukosis virus; APMV-1, avian paramyxovirus (Newcastle); IBDV, infectious bursal disease virus; IBV, infectious bronchitis virus; DHBV, duck hepatitis B virus; Salm, Salmonella enteritidis and S. typhimurium; Eim, Eimeria spp; Cl p, Clostridium perfringens; E coli, Escherichia coli; CAV, chicken anemia virus; ADV-1, avian adenovirus 1; REV, reticuloendotheliosis virus; M gall, Mycoplasma gallisepticum; ARV, avian reovirus; Afl, aflatoxins; Pm, Pasteurella multocida; APV, avian pneumo- virus; Fus, Fusarium spp; Och, ochratoxins. H-INDEX IN POULTRY DISEASES 6509 40 35 30 Percentage of citations 25 20 15 10 5 0 1910-1919 1920-29 1930-39 1940-49 1950-59 1960-69 1970-79 1980-89 1990-99 2000-09 2010-19 Decades Figure 4. Citations (in percentages) per decade of the publications included in the H-index cores based on taxonomic groups. Virus (blue), Bacteria (green), and Other (brown). index scores in our study—significantly higher H-in- contribution to their impact (McIntyre et al., 2014). dexes were only observed for OIE-listed Bacteria and Instead, our searches were carefully undertaken to zoonotic Others. Nevertheless, among the 20 highest only include studies with poultry species, thus ruling H-index scores, 45% were zoonotic and almost a third out any unwanted contribution from human studies. was OIE listed. Interestingly, Diaz et al. (2016) Roughly half of the 20 highest H-indexes were Viruses, observed that H-indexes of nonzoonotic swine patho- and the other half were Bacteria and Other. Distinct rea- gens were significantly higher than those of zoonotic sons for the highest ranked pathogens in each category ones (Diaz et al., 2016), whereas others found no dif- could be made. First, avian influenza virus (H-index ferences in the H-indexes of OIE-listed vs. not OIE- 127) is an economically devastating disease that affects listed animal pathogens (McIntyre et al., 2014; poultry worldwide, with its highly pathogenic (HP) Murray et al., 2016). Previously, significant differences form being able to cause 100% mortality rates between H-indexes for human-only, zoonotic, and (Spickler et al., 2008; Pantin-Jackwood and Swayne, animal-only pathogens in Europe (ranked in this or- 2009; Swayne et al., 2020a,b). Additionally, goose/ der) indicated that this single measure could be a Guangdong-lineage H5N1 and Anhui-lineage H7N9 of One Health metric accounting for such factors avian influenza viruses are among the most high-profile (McIntyre et al., 2014). However, McIntyre et al. zoonotic diseases (Collett, 2020). Second, S. enteritidis (2014) purposely included human and animal studies and S. typhimurium (as etiological agents of salmonel- in searches for zoonoses, overestimating the animal losis) (H-index 72) are 2 of the most common 100 90 80 70 60 Percentage 50 40 30 20 10 0 Europe North America Asia Oceania Africa South America Figure 5. Distribution by continents of publications included in the H-index cores. Percentage of publications originating from the continent; total publications (n 5 3,184) (black), Virus publications (n 5 1,428) (blue), Bacteria publications (n 5 965) (green), and Other publications (n 5 791) (brown). Values above bars are absolute number of publications. 6510 BERTRAN ET AL. nontyphoidal serovars isolated from humans (Gast and Other (n 5 47) Dcos-index: number of publications that a country holds within the set of publications included in the H-index core of a given subject (Diaz et al, 2016). For example, the USA holds 524 publications in the field of Total number of publications (TNP), percentages (%), and ranking for total publications. Of the 3,184 total publications included in the H-indexes searched for 111 pathogens, 1,428 publications belonged to Three-letter country codes were used (International Organization for Standardization [ISO]: Online Browsing Platform, 2020). GBR is used for the UK, United Kingdom of Great Britain, and Northern Ireland Porter, 2020). Although they only cause clinical disease 243 (30) 61 (25) 40 (20) 15 (10) 26 (10) 61 (22) 23 (10) 9 (6) 9 (8) 9 (4) in highly susceptible young birds exposed to stressful conditions (Gast and Porter, 2020), numerous studies in birds are probably aimed at understanding potential routes of transmission to humans and ultimately prevent Bacteria (n 5 33) zoonoses. Finally, Eimeria spp (H-index 70) is respon- 268 (31) 130 (25) 28 (13) 49 (21) 70 (16) 61 (17) 40 (16) 32 (15) 30 (13) 27 (13) sible for coccidiosis in poultry, one of the most common and economically important diseases of chickens world- wide (Cervantes et al., 2020). Anticoccidial drugs and Dcos-index2 vaccination are required for its control and, in recent years, consumer demand has fueled the development of Virus (n 5 31) alternatives to ionophores, a class of antibiotics for 524 (30) 172 (24) 136 (20) 83 (18) 33 (15) 62 (15) 35 (15) 47 (12) 29 (9) 3 (3) coccidiosis prevention (Cervantes et al., 2020). Interest- ingly, 6 of the 15 highest H-indexes belonged to patho- gens causing immunosuppression: avian leukosis virus, infectious bursal disease virus, Eimeria spp, chicken ane- Total (n 5 111) mia virus, reticuloendotheliosis virus, and avian 1,035 (91) 363 (74) 173 (39) 172 (59) 118 (41) 116 (36) 104 (39) 103 (38) 88 (38) 83 (29) reovirus. This is especially relevant because immunosup- pression not only predisposes birds to infection by other agents but also can hamper optimal response to vaccina- tion against any pathogen (Schat and Skinner, 2014). We note that some economically important diseases of Rank Publications in Other 18th 11th 18th 18th poultry had a relatively lower H-index than expected, 2nd 4th 5th 3rd 7th 1st such as the herpesvirus-induced Marek's disease (H-in- dex 33), mostly because of the exclusion of publications 30.7 7.7 1.1 5.1 1.9 3.3 7.7 1.1 2.9 1.1 % not strictly involving poultry species. The evolution of citations reflected severe poultry out- TNP 243 61 40 15 26 61 23 9 9 9 breaks and/or zoonotic outbreaks in relatively wide geographic areas, as previously observed for swine (Diaz et al., 2016). The most striking example was the Rank Table 4. Top 10 countries and continents of origin of all publications included in this study. 10th 11th 2nd 6th 3rd 4th 7th 8th 9th 1st Virus (31 pathogens), 965 publications to Bacteria (33 pathogens), and 791 to Other (47 pathogens). abrupt increase of avian influenza virus citations between Publications in Bacteria 2002 and 2009, as a result of the emergence of goose/ 27.8 13.5 2.9 5.1 7.2 6.3 4.1 3.3 3.1 2.8 % Guangdong-lineage H5 HP avian influenza virus in China in 1996 that subsequently spread to 4 continents, repre- TNP senting a major HP avian influenza panzootic (Sims 268 130 28 49 70 61 40 32 30 27 and Brown, 2016). The polar opposite was avian leukosis virus, which citations stalled in 1997. Avian leukosis virus Rank Publications in Virus 40th 2nd is the most common leukosis sarcoma group of retrovi- 3rd 4th 8th 9th 5th 7th 6th 1st ruses associated with neoplastic diseases in poultry (Nair et al., 2020). They were the first neoplastic diseases 36.7 12.0 9.5 5.8 2.3 2.0 0.2 4.3 2.4 3.3 % in any species to be shown, more than 100 yr ago, to be viral-transmissible and have consequently been studied Viruses, which include 30 of the 31 virus pathogens analyzed. TNP 3 524 172 136 83 33 29 62 35 47 extensively by biomedical scientists as models for the role of viruses in cancer (Payne and Nair, 2012). In the EU, Europe; NA, North America; OCE, Oceania. Rank 1920s, they also became the major cause of mortality (England, Scotland, Wales, and Northern Ireland). 10th 2nd 3rd 4th 5th 6th 7th 8th 9th Total publications1 1st and economic loss to the developed poultry industry and were thus studied by agricultural scientists searching 3.23 5.4 5.4 3.7 3.6 3.3 2.8 2.6 32.5 11.4 % for control methods (Payne and Nair, 2012). The decrease in research production since the turn of the cen- tury could be related to the fact that meat-type broiler 1,035 363 173 172 118 116 104 103 88 83 TNP breeders and broilers have been generally free of avian leukosis virus for the last decades in western countries 4 Continent thanks to rigorous, well-tested eradication programs. ASIA ASIA OCE Even if the disease remains and has spread to layer flocks NA NA EU EU EU EU EU in other countries, notably China (Payne and Nair, 2012), the impact of more recent publications on avian 3 leukosis virus is not sufficient as to be included in its H-in- Country dex core. We note that, since time is needed to accumu- DNK CHN CAN GBR DEU NLD FRA AUS USA JPN 1 2 3 4 late citations and increase the H-index, more recently H-INDEX IN POULTRY DISEASES 6511 emerged pathogens are in a disadvantageous situation. The H-indexes are a delayed reflection of changes in Such is the case of Gallibacterium anatis, duck egg drop regulations, as aforementioned, and in investment prior- syndrome virus, Helicobacter pullorum, Salmonella ari- ities over the past decades. One of the limitations of this zonae, C. hepaticus, and C. gallinacea, all of them with study is that, because the most recently available R&D H-indexes below 23 (data not shown). budgets were analyzed, their effect will only be seen in The evolution of citations based on taxonomic groups the years to come and do not necessarily explain the evo- mirrors major changes in poultry production practices lution of H-indexes and citations of the past decades. We and management throughout history. On the one speculate that China will soon surpass USA and other hand, Others were the most cited pathogens in the H-in- countries in number of publications and will be included dex cores until the 1970s and, following 3 decades of un- among the top countries of origin of publications in the popularity, regained importance in the 2000s. Since the H-index core of the highest H-indexed pathogens (as of widespread use of modern production practices, and now, China is only shortlisted as second contributor especially modern caging, in the 1970s, internal and for avian influenza virus). Also, we recognize that external parasite exposure in intensively reared flocks knowing the percentage of R&D dedicated to poultry had significantly reduced and only been maintained in or animal health would allow for more accurate backyard flocks (Murillo and Mullens, 2016; Hinkle conclusions. and Corrigan, 2020). Reversion to husbandry practices Because the EU block has produced antibiotic-free that restore environmental conditions conducive to par- poultry for longer than other continents, research on asites, as has been demonstrated in European practices Bacteria control has been a greater priority than in since 2000, has allowed a resurgence of poultry pests other regions. Similarly, most African and South that had not been seem as problematic in commercial American countries with a great proportion of back- production for over 50 yr, such as the poultry red mite yard holdings and farms with low biosecurity stan- (Hinkle and Corrigan, 2020). As welfare regulations dards consequently exhibit high incidence of parasites become ever more stringent in the years to come, Others (some of them geographically restricted) and contrib- are expected to maintain and even increase in relevance. uted disproportionately to H-indexes of Other On the other hand, citations for Bacteria increased espe- (Diaz et al., 2016). Pathogens that affect chickens cially in the 1990s and surpassed Viruses from the 2000s ranked the highest in H-indexes, irrespective of to date. EU-wide limitations on antimicrobial use began whether they also affect turkeys, ducks, and/or geese, in 1997 with the ban of the growth promotion use of avo- whereas diseases that present host restriction to spe- parcin, and by 2006, the remaining growth promoters cies other than chickens had an insignificant relevance were removed (U.S. Government Accountability Office, (data not shown). This can be because of the great 2011; Maron et al., 2013). A similar prohibition in the importance of chickens in poultry—thanks to their USA followed a decade later, when the FDA banned high feed-meat conversion ratio and egg production, growth-promoting and other nontherapeutic uses of anti- broilers and layers are the birds mainly produced by biotics in 2017 (U.S. Food and Drug Administration, modern integrated poultry facilities to meet growing 2020). As a consequence of these regulatory changes, global demand for animal-source foods. western and other countries have faced increasing chal- In conclusion, the H-index could be a valid tool to pri- lenges in the control of bacterial and protozoal infections, oritize funding or interest in poultry diseases, and the and more research has been devoted to nonantibiotic evolution of the H-index of a particular pathogen may medications and preventive measures, such as changes be used to identify major poultry outbreaks or zoonotic in management and diet, use of chemically synthesized events. However, because of its intrinsic limitations, coccidiostats, and probiotics (Collett, 2020). Collec- the H-index should be used as a preliminary selection tively, both welfare and medication regulations seem to approach in combination with other metrics, such as be shifting control priorities toward diseases previously severity of disease, economic impact, trade bans, food recognized as unimportant but that are now re- insecurity, and zoonotic potential. emerging as significant concerns (Collett, 2020). The socioeconomic framework can influence the research contribution of a particular country or conti- ACKNOWLEDGMENTS nent. China and the USA not only topped poultry pro- ductions but also had the largest R&D budgets, with The authors would like to thank all the researchers figures around $5.10 x 1011. Japan, Germany, France, that have contributed with their effort and dedication and the UK ranked among the highest 10 R&D budgets to the advancement of poultry health. K.B. is funded and also made the list of top countries of origin of publi- by the Generalitat de Catalunya, Spain, Agencia de Ges- cations for many pathogens. The USA exhibited, by far, tio d’Ajuts Universitaris i de Recerca, Beatriu de Pin os the strongest poultry research production not only in postdoctoral fellowship (2017 BP 00105). M.C. is funded number of publications but also in the diversity of path- by the Ministry of Economy and Competitiveness, ogens studied, according to Dcos-index. Interestingly, Spain, program Ramon y Cajal (grant RyC-2015- the UK followed the USA in Dcos-index, despite falling 17154). This research did not receive any specific grant behind other countries in poultry production and R&D from funding agencies in the public, commercial, or budget. not-for-profit sectors. 6512 BERTRAN ET AL. Conflicts of Interest Statement: The authors declare McIntyre, K. M., C. Setzkorn, P. J. Hepworth, S. Morand, no conflicts of interest. A. P. Morse, and M. Baylis. 2014. 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