A Global Perspective of Vibrio Species and Associated Diseases: Three-Decade Meta-Synthesis of Research Advancement

Abstract

Outbreaks of Vibrio infections have a long history of global public health concern and threat to the aquaculture industry. This 3-decade (1990-2019) meta-synthesis of global research progress in Vibrio species and associated disease outbreaks was undertaken to generate the knowledge needed to design effective interventions with policy implications. Using PRISMA protocol, we obtained data on the online version of the Institute for Scientific Information (ISI), Web of Science (WOS), and Scopus from January 1990 to September 2021 by title search of the keywords “Vibrio species OR Vibrio spp. OR vibriosis.” On the 3-decade survey, the result has shown that a total of 776 publications document types were published on the subject, with an average of 24.25 ± 13.6 published documents per year with an annual growth rate of 4.71%. The year 2020 recorded the highest output of 52 published documents accounting for 6.70% of the total. The most prolific author, Blanch A., published 12 articles on the subject and has received citations of 1003 with an h-index of 10. While the most global cited paper author is the journal of J. Bacteriol (Bassler et al), receiving total citation (TC) (550) and per Year (22). The top active corresponding authors country is the United States of America with (92) articles, freq. 12.40%; TC of 3103. The observations in this study, such as the collaborations network map, and index, which have outlined a big difference between countries based on economic status, have underscored the need for a sustained research mentorship program that can define future policies.

Keywords

Global perspective meta-synthesis

Introduction

The members of the Vibrio genus are spread worldwide, being autochthonous in marine, coastal, and riverine environments.^1,2 Some Vibrio species (Vibrio spp.) are potentially pathogenic and lives freely in the surface waters. Ample studies have been done on Vibrio cholerae, the etiologic agent of cholera.^3
-6 There is scanty information on other human pathogenic Vibrio spp., including the emerging vibriosis of economic importance such as those caused by Vibrio fluvialis and Vibrio mimicus.^3,7
-9 Human pathogenic Vibrio cause: foodborne illness, outbreaks, watery diarrheal, gastro-intestinal disease, septicemia, and wound infections.^6,10 These are usually associated with the use of contaminated water, and eating contaminated undercooked seafood. Vibrio spp., are Gram-negative, comma-shaped bacteria that occur naturally in the aquatic environment, and they possess a single polar flagellum for motility.^11,12 In water, their abundance is associated with temperature, salinity, the concentration of organic matter and the presence of zooplankton,^3,13,14 which enable the genus to survive in both culturable and non-culturable^15,16 form. Most Vibrio infections occur during the summer and decline during winter. Hygiene and water quality are positive contributing factors to the public health burden of vibriosis.^14,17
-19 Vibrio was first reported in 1718 by Colwell and Grimes 1984.²⁰ It was reported as Vibrio infection in fishes by Canestrini 1893. It became a threat to fish farming in North America, Europe, and Japan.²¹ Infections by Vibrio spp., are named after their discoveries (winter ulcer disease caused by V. viscosus named after moritella viscosa, Vibrio wodanis named after aliivibrio wodanis). Investigations have implicated dozens of Vibrio genera in human disease conditions.^19,22,23 The human pathogenic Vibrio spp. of clinical relevance include Vibrio (V.) parahaemolyticus, V. cholerae, Vibrio vulnificus, V. tubiashi, and V. fluvial, which are transmitted via contaminated water and seafood. Also, V. parahaemolyticus, V. vulnificus, and V. mimicus are foodborne pathogens.²⁴ The halophilic, V. alginolyticus, V. fluvialis, and V. metschnikovii are human pathogenic,¹⁹ while V. anguillarum, parahaemolyticus, alginolyticus, vulnificus, harveyi, and others are also potentially pathogenic to aquatic animals.^19,23,25 Over 100 species of the Vibrio genus have been found in surface waters, estuarine, and marine bodies, with the unending list due to discovering new potential pathogenic species.^2,26,27 Among the health conditions associated with human pathogenic Vibrio spp. of significant health concern is cholera infection characterized by painless watery diarrhea and vomiting.^28,29 World Health Organization (WHO) classified 51 countries endemic to cholera in 2017. About 1.4 to 4.3 million cholera cases occur worldwide every year, with a mortality rate ranging from 28 000 to 142 000. Low and middle income countries share an enormous two-thirds volume. Sub-Saharan Africa is one endemic region with sporadic high mortality of malaria,³⁰ human immunodeficiency virus/acquired immunodeficiency syndrome (HIV/AIDS)³¹ and cholera infection.^32,33 Uganda is one of the 51 endemic countries where cholera outbreaks^28,34
-36 is still very rampant. Uganda has suffered repeated cholera cases and deaths since 1998^33,37,38 communities most vulnerable to cholera outbreaks in Uganda are situated along the lakes.^3,32,39,40 Lack of safe drinking water and poor sanitation contribute to the high cholera burden in Uganda, where 8% of people depend on surface waters for commercial/domestic and agricultural uses while 7% do not have access to proper basic sanitation.⁴¹ The burden of cholera outbreaks is worst along the Western border with the Democratic Republic of Congo (DRC), the Karamoja region to the north, and Kampala city slums.²⁸ Surprisingly, there is a lack of regular surveillance and research to monitor the presence of potentially pathogenic species of Vibrio spp. on water bodies in this region.

V. parahaemolyticus is not an invasive pathogen; they take advantage of breached barriers and cause infection primarily affecting the colon, causing gastroenteritis.^4,24,42 V. parahaemolyticus and V. vulnificus cause wound infection and sepsis in the blood²⁴ and are the 2 most common Vibrio infections reported in the United States between 1997, States between 2006. V. vulnificus infections account for 95% of Vibrio related deaths in the United States.⁹ V. fluvialis is pathogenic to fish and crustaceans.^10,23 V. fluvialis causes gastroenteritis and extraintestinal infections, such as hemorrhagic cellulitis and cerebritis,⁴³ peritonitis,⁴⁴ acute otitis,^45,46 biliary tract infection,⁴⁷ bacteremia,⁴⁸ and even ocular infections.⁴⁹ V. mimicus had been implicated with sporadic cholera-like diarrhea.⁵⁰ V. anguillarum is the causative agent of a fatal hemorrhagic septicemic disease that also infects fish, mollusks, and crustaceans.^{9,19,25,51,52} V. alginolyticus is an opportunistic halophilic (grow in 10% NaCl) vibriosis^19,53 and causes septicemia and skin ulcers.^9,19,25,52 Also implicated in gastroenteritis, otitis media, wound infection, and endophthalmitis.^10,19,54
-57

There is no updated report of outbreak incidence, especially in low resource settings and on other potentially pathogenic species. Surveillance and incidence of other vibriosis-related foodborne diseases, outbreaks, gastroenteritis, and extraintestinal infections remain poorly reported.¹ Despite the progress in Vibrio spp., research, there is a dearth of knowledge needed to reduce the foodborne and waterborne hazard burden posed by the pathogens. The outcome and recommendation of 3-decade research in Vibrio species and associated diseases summarized in 1 paper will be profoundly significant to the stakeholder and policy markers in a combined effort to mount effective intervention. This study will also help health care providers and planners in developing country settings to harmonize available skills to harness limited resources in designing and implementing effective control.

In this review, we map and evaluate the relevant titled publication documents (PD) for a 3-decade global analysis of activities to reveal the cooperation network map among various countries, institutions, and individuals on the Vibrio spp. research in order to suggest the scientific reference for the establishment of the relevant policy.

Methods

Data retrieval

Specific title published articles on Vibrio spp., between January 1990 and September 2021, were retrieved from online version 5.34 of the ISI (Institute for Scientific Information) Web of Science and Scopus databases of a rapid science citation index (SCI) of a multidisciplinary database. The keywords “Vibrio species OR Vibrio spp* OR vibriosis” were the title-specific search terms for documents within the timespan 1990 to 2021 following PRISMA guidelines.^58,59

On December 31, 2019, the complete metadata for each original published article was collated and updated on September 15 2021, from Web of Science and Scopus databases. Titles and abstracts were reviewed for relevance by 2 independent authors, and papers judged relevant by 1 author were assessed in full by both authors. The title search yielded 776 document types extracted and imported in BibTxt, and CSV file formats, then normalized using ScientoPy R-package,⁶⁰ and duplicates were removed using bibliometric and fBasics R-package^61,62 on Rstudio versions 4.0.5,^61,63 as shown in Figure 1.

Figure 1.

PRISMA process of searching, reviewing, and selecting research articles.

Data processing and analysis

To import and manage the metadata from Web of Science and Scopus, we utilized bibliometrix version 1.7,⁶¹ an R-Tool of R-Studio version 4.0.1⁶³ for comprehensive science mapping analysis, and biblioshiny, the shiny interface offering a web interface for bibliometrix. The main characteristics, scientific production, author’s impact, corresponding author’s country, most cited countries, sources impact, most global cited documents, the total number of publications, citations count with total citations (TC), average article citations (AAC), the number of citing articles, journal sources, keywords, countries/regions, and author-level metrics such as h-, m-, and g indexes were all included in the baseline metadata analysis. H-index measures the number of papers published with at least 1 citation.^64,65 It is often used to evaluate the impact of a scientist on his or her peers. The m-index or m-quotient (ie, the h-index divided by the number of years from the author’s first publication [m-quotient = h-index/n, n = number of years since the scientist’s first published article]) was used since the h-index does not consider the author’s career span. Furthermore, the g-index, which grants credit for the most highly cited papers in a data set, was also employed to account for the citation evolution of the most cited works of a specific author over time. The annual growth rates of scientific publications were calculated by applying a calculator (CAGR) at www.investopediacom.com/calculator.

The authors, institutions and countries network analyses were used as collaboration indicators. In addition, the keywords network from the bibliographic data collection was used to map the conceptual structure framework with a dimensionality reduction technique and Multiple Correspondence Analysis (MCA), which are connected in groups of papers expressing similar ideas. Categorical variables were reported as frequency and percentage, and continuous datasets were presented as medians with maximum and minimum values.

Results

Global publication performance and growth rate on a 3-decade survey of Vibrio spp., research Landscape

A global evolution trend of research titled Vibrio spp., a 3-decade timespan study, was carried out. A total of 1299 documents were published during the survey period, while 776 research articles types were included in this review, and their characteristics are presented in Table 1. We obtained a collaboration index of 3.81, which implies moderate involvement of co-authorship per document^16,66,67 and 2917 authors per document of 3.76 and co-authors per document of 5.12. Citations per document were 24.7 on average. Fourteen (14) authors were involved in single-authored documents, while 2903 authors were involved in multi-authored documents. The values obtained from the present study suggest a positively skewed distribution of citations of a single author and multiple authors among the published documents in this study.^68,69

Table 1.

Descriptive data of retrieved information on Vibrio spp.

Description	Results
Timespan	1990:2021
Sources (Journals, Books, etc)	290
Documents	776
Average years from publication	11
Average citations per document	24.7
Average citations per year per doc	2.113
References	25606
Document types
Articles	776
Document contents
Keywords Plus (ID)	4407
Author’s Keywords (DE)	1581
Authors
Authors	2917
Author Appearances	3974
Authors of single-authored documents	14
Authors of multi-authored documents	2903
Authors collaboration
Single-authored documents	14
Documents per Author	0.266
Authors per Document	3.76
Co-Authors per Documents	5.12
Collaboration Index	3.81

The results depict a rapid increase of research articles in some years of the study period with fluctuations in overall production between 1990 and 2021. There was a tremendous increase in PD in 2010 (n = 37) compared to the previous years in the first 2 decades. In 2012 (n = 28), PD dropped in the third-decade survey with a rising gain of 52 in 2020. The mean of total citation per article (meanTCperArt) is depicted through a line graph plotted on the secondary axis indicating 1999 published documents receive the highest mean citation of 89.4, as presented in Figure 2. The result shows that the rapid increase beginning from the end of the second decade (2000-2010) may be primarily due to the seafood outbreak associated with Vibrio spp., specifically, V. parahaemolyticus and V. vulnificus 2009 to 2010 in a developed country such as the USA, developing nation Mexico, and mid-range economy Spain. More specifically, developed countries with high per capita income are expected to control their disease and outbreaks better than developing countries.^70,71 Thus, during the seafood disease outbreak, the developed country, (USA) should usually control the outbreak better than Spain, and Mexico, lending credence to the role of economic status as a driver of effective disease control programs.^70,71 Articles in the first decade (1990-2000) gain more citations than other decades due to high-quality journals and considerable years of publication. The citable year continues to decline from 1990 (30) to 2020 (3) and is lower than the previous years because most freshly published publications had not been cited extensively at the time of data extraction for our analysis. However, over the last 30 years, the results revealed 2 distinct growth dynamics: increasing article production and decreasing mean TC per articles, as it takes time for new studies to gain appreciable citations.

Figure 2.

Three-decade scientific research output on Vibrio spp. and associated infections.

The total number of publications per year, mean total citation per year and articles, and citations years, with an annual growth rate of 4.71%.

The 3-decade evolution survey of authors productive on Vibrio spp

The most productive researchers in the evolution of Vibrio spp., studies revealed 2 prolific authors, Blanch A from the University Barcelona in Spain and Kim Y of the Pukyong National University in South Korea, shared the first position with (nPD = 12; 1.55%), and h-index of 12, 7 respectively. Also, where the most impactful authors among the top 20 productive authors. The ranking was based on the number of published articles in the studied period. The second leading author is Kim H of the Yonsei University in South Koran with (nPD = 11 1.42%) and an h-index of 7, while the third prolific author is Kim J of the Sogang University in South Koran (nPD = 10; 1.29%) and an h-index of 6 as indicated in Table 2.

Table 2.

Published documents and research impact of top 20 authors in this survey.

Ranked	Element	PD	h_index	g_index	m_index	TC	PY_start
1	Blanch A	12	10	12	0.357	1003	1994
1	Kim Y	12	7	12	0.304	495	1999
2	Kim H	11	7	11	0.269	207	1996
3	Kim J	10	6	9	0.316	91	2003
5	Gomez-Gil B	9	7	9	0.292	500	1998
6	Kim M	9	5	7	0.192	62	1996
7	Wang Y	9	7	9	0.389	181	2004
8	Choi S	8	7	8	0.438	255	2006
9	Lee K	8	8	8	0.5	236	2006
10	Colwell R	7	7	7	0.35	228	2002
11	Kong I	7	6	7	0.4	105	2007
12	Lee J	7	6	7	0.5	85	2010
13	Lee S	7	6	7	0.3	145	2002
14	Nishibuchi M	7	7	7	0.226	731	1991
15	Okoh A	7	5	7	0.357	178	2008
16	Oliver J	7	7	7	0.304	307	1999
17	Wang X	7	4	7	0.182	65	2000
18	Zhang X	7	5	7	0.294	72	2005
19	Igbinosa E	6	5	6	0.357	172	2008
20	Jung Y	6	6	6	0.857	75	2015

Abbreviations: PD, number of published documents; TC, total citation.

Ranked based on the PD.

The most cited papers on Vibrio spp., global research survey, are shown in Table 3. The paper author by Bassler BL, 1997, published in J Bacteriol, has received a TC and TC per Year of (550 and 22) emerged as the most cited study. Seconded by Kim YB, 1999, published in J Clin. Microbiol. (387 and 16.82). Alsina M, 1994, published in J Appl. Bacteriol. been the third most cited study in the survey with TC and TC per year of (285 and 10.18). Due to the importance of vibriosis to public health, research related to this illness has been widely accepted in established and reputable journals. However, researchers tend to cite papers in high-impact factor journals more often than those in other journals. This is because these papers are more detailed and influential.

Table 3.

The most cited papers on Vibrio spp., in this survey.

Paper	TC	TC per year
Bassler et al,⁷² J Bacteriol.	550	22
Kim et al,⁷³ J Clin Microbiol.	387	16.82
Alsina and Blanch,⁷⁴ J Appl Bacteriol.	285	10.18
Nandi et al,⁷⁵ J Clin Microbiol.	270	12.27
Alsina and Blanch,⁷⁴ J Appl Bacteriol.	251	8.96
Kirstein et al,⁷⁶ Mar Environ Res.	236	39.33
Vaseeharan and Ramasamy,⁷⁷ Lett Appl Microbiol.	221	11.63
Brackman et al,⁷⁸ Bmc Microbiol.	199	14.21
Hikima et al,⁷⁹ Gene	163	8.58
Panicker et al,⁸⁰ Appl Environ Microbiol.	156	8.67
Cervino et al,⁸¹Appl Environ Microbiol.	141	7.83
Adams,⁸² Fish Shellfish Immunol.	138	4.45
Baker-Austin et al,⁸³ Nat Rev Dis Primers	132	33
Okuda et al,⁸⁴Microb Pathog.	125	4.63
Porsby et al,⁸⁵ Appl Environ Microbiol.	121	8.65
Zorrilla et al,⁸⁶J Fish Dis.	117	6.16
Gomez-Gil et al,⁵⁴ Aquaculture	115	4.79
Gopal et al,⁸⁷ Int J Food Microbiol.	114	6.71

The evolution of corresponding author’s countries and most cited countries of the 3-decade global survey on Vibrio spp., research

Table 4 shows the various countries that participated in the Vibrio spp., global research survey. The USA is associated with 92 articles. Out of these, 87 were single country publications (SCP), and only 5 were multiple country publications (MCP). Similarly, developing countries such as China (77, 70, 7) and India (62, 61,1), while Japan (56, 52, 4); South Korea (51, 49, 2); Spain (44, 40,4) were the top productive corresponding author’s country. The frequency of publications among the top countries ranges from 12.40% to 5.93%. At the same time, the USA top in country total citation (TC) (3103) and average articles citation (AAC), 33.73 followed by Japan (2083; 37.2), Spain (1767; 40.16) India (1585; 25.56), China (1280; 16.62), Italy (1115; 30.97).

Table 4.

Corresponding author’s countries and most cited countries on this survey.

Corresponding author’s country						Most cited countries
Country	nPD	%Freq	SCP	MCP	MR (%)	Country	TC	AAC
USA	92	12.40	87	5	5.43	USA	3103	33.73
China	77	10.38	70	7	9.09	Japan	2083	37.2
India	62	8.36	61	1	1.61	Spain	1767	40.16
Japan	56	7.55	52	4	7.14	India	1585	25.56
South Korea	51	6.87	49	2	3.92	China	1280	16.62
Spain	44	5.93	40	4	9.09	Italy	1115	30.97
Italy	36	4.85	25	11	30.56	Germany	853	32.81
Germany	26	3.50	21	5	19.23	South Korea	622	12.2
Brazil	22	2.97	21	1	4.55	Belgium	563	62.56
Mexico	22	2.97	19	3	13.64	United Kingdom	517	36.93
France	21	2.83	17	4	19.05	Brazil	487	22.14
Australia	20	2.70	19	1	5	Mexico	454	20.64
Malaysia	16	2.16	15	1	6.25	France	418	19.9
United Kingdom	14	1.89	10	4	28.57	Australia	360	18
Iran	13	1.75	13	0	0	Norway	336	42
Canada	12	1.62	11	1	8.33	Canada	251	20.92
Thailand	12	1.62	9	3	25	Denmark	221	44.2
South Africa	10	1.35	8	2	20	Thailand	201	16.75
Belgium	9	1.21	8	1	11.11	Tunisia	188	23.5
Nigeria	9	1.21	8	1	11.11	South Africa	185	18.5

Abbreviations: AAC, average articles citations; Freq, frequency; MCP, multiple country publications; MR%, MCP_Ratio %; nPD, number of published documents; SCP, single country publications; TC, total citations.

The most relevant sources of the 3-decade global survey on Vibrio spp., research

The top academic journals publishing papers relevant to Vibrio spp., research in the survey period are presented in Table 5. Applied and Environmental Microbiology top the list of journal sources impact 46 articles, 2136 citations, and an h-index of 28. Similarly, Aquaculture (20; 399 and 11), Journal of Applied Microbiology (20, 649, and 15), Journal of Food Protection (18, 359, and 12), Journal of Bacteriology (17, 1149, and 13), and Letters in Applied Microbiology (15 articles, 408 citations, and 7 h-index) respectively.

Table 5.

Most relevant journal sources on Vibrio spp., research.

Sources	PD	h_index	g_index	m_index	TC	PY_start
Applied and Environmental Microbiology	46	28	46	0.87	2136	1990
Aquaculture	20	11	19	0.37	399	1992
Journal of Applied Microbiology	20	15	20	0.6	649	1997
Journal of Food Protection	18	12	18	0.38	359	1990
Journal of Bacteriology	17	13	17	0.42	1149	1991
Letters in Applied Microbiology	15	7	15	0.24	408	1993
Journal of Fish Diseases	14	8	14	0.27	300	1992
Food Control	13	10	13	0.5	345	2002
Systematic and Applied Microbiology	13	9	13	0.32	429	1994
Microbial Ecology	12	10	12	0.31	386	1990
FEMS Microbiology Letters	11	8	11	0.28	220	1993
International Journal of Food Microbiology	11	8	11	0.33	471	1998
Plos one	11	7	11	0.64	211	2011
Scientific Reports	10	6	10	1	228	2016
Journal of Microbiological Methods	9	4	9	0.17	83	1998
Microbial Pathogenesis	8	6	8	0.22	334	1995
BMC Microbiology	7	7	7	0.5	387	2008
FEMS Microbiology Ecology	7	6	7	0.21	280	1994
Fish and Shellfish Immunology	7	6	7	0.19	379	1991
Frontiers in Microbiology	7	6	7	0.86	133	2015

Table 6 lists the most frequently keywords used in the 3-decades global survey on Vibrio spp., research including both author keywords (AK) and Keywords-Plus (KP). Five among the top 20 keywords found in publications about Vibrio spp. research in the author keywords includes: Vibrio (n = 608; 78.35), vibriosis (n = 283; 36.47), Vibrio parahaemolyticus (n = 281; 36.21), Vibrio cholerae (n = 275; 35.44), non-human (n = 235; 30.28), Vibrio vulnificus (n = 193; 24.87). While the 5 top KP includes; Vibrio (n = 158; 20.36), Vibrio spp., (n = 69; 8.89), Vibrio parahaemolyticus (n = 48; 6.19), Vibrio cholerae (n = 35; 4.51), Vibrio species (n = 29; 3.74).

Table 6.

Top 20 most relevant keywords related to Vibrio spp. on this survey.

S/N	keyword plus	Occurrences		Authors keywords	Occurrences
1.	Vibrio	608	78.35	Vibrio	158	20.36
2.	Vibriosis	283	36.47	Vibrio spp	69	8.89
3.	Vibrio parahaemolyticus	281	36.21	Vibrio parahaemolyticus	48	6.19
4.	Vibrio cholerae	275	35.44	Vibrio cholerae	35	4.51
5.	Nonhuman	235	30.28	Vibrio species	29	3.74
6.	Vibrio vulnificus	193	24.87	Vibrio vulnificus	25	3.22
7.	Bacterial	130	16.75	Aquaculture	23	2.96
8.	Controlled study	124	15.98	Vibriosis	23	2.96
9.	Priority journal	122	15.72	Shrimp	22	2.84
10.	Polymerase chain reaction	119	15.34	PCR	21	2.71
11.	Bacteria (microorganisms)	116	14.95	Virulence	20	2.58
12.	Vibrio alginolyticus	114	14.69	Vibrio harveyi	18	2.32
13.	DNA	110	14.18	Antibiotic resistance	17	2.19
14.	Animals	98	12.63	Multiplex PCR	17	2.19
15.	Microbiology	98	12.63	Identification	16	2.06
16.	Parahaemolyticus	97	12.50	Seafood	15	1.93
17.	Phylogeny	97	12.50	Vibrio alginolyticus	15	1.93
18.	Genetics	92	11.86	Vibrios	15	1.93
19.	Virulence	81	10.44	Fish	14	1.80
20.	Vibrio harveyi	79	10.18	Vibrio sp.	14	1.80

Abbreviations: DNA, deoxyribonucleic acid; PCR, polymerase chain reaction; spp/sp, species; V, Vibrio.

The 3-decade global use of keywords and topic/stream on Vibrio spp., research survey

The K-means clustering shows 4 clusters of 4 thematic concepts frequently linked to Vibrio spp., research. The thematic conceptual landscapes in Vibrio spp., research are shown in Figure 3. The identified 4 conceptual thematic frameworks (CTF) includes: CTF#1 (green cluster), involving the sequences analysis, nucleotide sequence, Vibrio strain/bacterial protein and genes, phylogeny as the modern bacterium evolution to understand vibriosis pathogenicity. This cluster received the most excellent attention. The pathogenic strain pointed in CFT#1 is V. mimicus. The conventional detection methods involve DNA extraction and sequencing genomes for genetic examination. In addition, therapeutic management includes unclassified drugs. The second CTF#2 highlights the emerging strains of public concern. The strains mentioned are V. alginolyticus, harveyi, vulnificus, parahaemolyticus, and cholerae and their molecular characterization by polymerase chain reaction (PCR). These species are implicated in several infectious diseases, food poison and outbreaks due to their expression of virulence toxins example, V. parahaemolyticus, cholerae. Also, they are widely distributed in aquaculture, water and seafood. Third, CTF#3 centered on the pathogenicity to humans, animals and the microbiological methods of isolation and purification. The 4 cluster CTF#4 focuses on identifying the pathogenic V. parahaemolyticus and vulnificus.

Figure 3.

Research topics and conceptual landscapes on Vibrio spp.

Figure 4, shows the collaboration network between; (A) Authors, the author’s name is represented by a circle, with the size of each circle indicating the total number of publications present in the network collaboration with other authors. Connecting lines represent collaboration pathways between authors. The thick/bold lines and names indicate the highest number of collaborations and co-authorships. (B) Institution, each institution is represented by a circle, with the size of each circle indicating the total number of publications connected with interlinked pathways lines networks. The thickest lines and names represent the institutions with greater strength in collaborations with other institutions. (C) Countries, each nation is represented by a circle, with the size of each circle indicating the total number of publications connected with interlinked pathways lines networks; the thickest lines and names represent the nations with more outstanding strength in collaborations with other countries

Figure 4.

The top authors’ (A), institutions (B), and countries (C) collaboration and coupling networks on Vibrio spp., research.

Discussions

This study’s findings reveal that the number of publications, contributing countries, and the average number of authors per document increased over time on the subject of Vibrio spp. However, the number of countries that made significant contributions was restricted to developing countries, as was the average number of citations per document and the number of publications that made significant contributions. Vibriosis mainly was linked to the consumption of contaminated water and the consumption of raw/undercook seafood. Most of the literature at the community level, region, and nation focused on the isolated/characterization of strains’ prevalence, dispersion, pathogenicity, and antimicrobial resistance, in response to the increasing reports of outbreaks, infections associated with potentially pathogenic Vibrio spp., and the emergence of its antimicrobial resistance (AMR) problem.^59,88 The reoccurring and unending global epidemic of Vibrio spp., requires a resolution urging member states to develop and adopt a stringent strategy that promotes and minimizes outbreaks and infection and also promote policies to reduce the spread of its resistant strains in the environments. Therefore, this survey aims at arousing the attention of many countries, investigators, academics, and policymakers.

WHO report on the first global burden of foodborne diseases in 2015 show that about 1 in every 10 people worldwide is sickened by the foodborne disease each year, and Vibrio spp., is one of the principal causes. It affects 600 million people, of which 420 000 die due to foodborne disease. It is imperative to note that diarrheal disease agents are number 1 among the 31 foodborne hazards global estimates by WHO.⁸⁹ Diarrheagenic agents include Campylobacter spp., Cryptosporidium spp., Entamoeba histolytica, norovirus, non-typhoidal Salmonella, pathogenic E. coli, Vibrio spp., (V. cholerae, V. parahaemolyticus, V. vulnificus, V. mimicus).^89,90 However, new scientific knowledge is rapidly driving health emergency outbreaks of infection on emerging viral pathogens (Zika, Chikungunya, Ebola viruses, and the likes), reflecting a significant increase in the number of research publications on these subjects.⁹¹ For instance, the Chikungunya virus records only 8 publications in 2005 but gained a significant upsurge to 302 by 2014.⁹² In the same vein, the Ebola virus had 43 publications in 2013 prior to the Ebola outbreaks in West Africa, and by 2014 has increased to more than 600 publications in 2014,⁹³ advancing knowledge in these subjects granting directives to policy markers.

The topmost active authors regarding h_index (total citations) were affiliated with institutions in developed nations, including the USA, Germany, Japan, South Korea; developing nations China and India; mid-economy nations Spain and Italy. This attribute is due to advanced technology and intense research coupled with funding to ensure the safety of drinking water, foods, and aqua agricultural products that are not contaminated with Vibrio spp. Interestingly, a Spanish researcher shares the first position spotlight with a South Koran researcher on Vibrio infection. This may be because the Vibrio outbreak in Spain and Mexico must have encouraged the Spanish researcher to do more research on Vibrio than others. It is unclear why USA authors are missing from the first position spotlight. This study has summarized the research findings that will advance our knowledge in Vibrio spp., pathogenicity. The magnitude of disease distribution and the rapidity of the onset, with the worldwide spread of disease associated with Vibrio spp. have been widely covered in this 3-decade study. Lineage and clade identity, molecular epidemiology, and global geographical niche directed distribution has been fully reported. Thus, our knowledge has been advanced, and we are better equipped to face the next generation challenges regarding Vibrio spp., and related infections.

Disease management programs are structured treatment plans that help people improve the management of chronic diseases on a long- and short-term basis. This requires an established health care system, resources, and policies to implement recommended interventions. High-income countries are expected to offer sustainable and more effective health delivery services than their middle or low-income countries counterparts. Therefore, it is safe to infer that a high-income country with the most necessary resources to implement health services will perform better than middle and low-income countries’ counterparts. Again, the Centers for Disease Control and Prevention (CDC) is the gold standard for a global disease control pattern. All counties have a CDC modeled after the CDC in the USA to mount a unified uniformed response again health emergencies.

In Africa, only 2 authors, Okoh A. I. (South Africa) and Igbinosa E. O. (Nigeria), were listed in the top 20 authors global 3-decade evolution survey of authors productive on Vibrio spp. This may indicate that many countries in Sub-Saharan Africa, among the 51 regions with endemic Vibrio cholera, gastroenteritis, septicemia, and hemorrhagic infections associated with other Vibrio spp., lack regular water surveillance. This may be due to a lack of research mentorship, technology/advances required or peradventure lack of funding. Even though this study report only 2 authors from Africa, there are studies about Vibrio spp. in Africa that are not limited to these 2 authors. There are studies done in Africa concerning Vibrio spp., probably without contribution from local investigators or the studies were published in journals not indexed in the 2 databases used for this review. Uganda, for instance, has experienced recurring episodes of V. Cholera outbreak from 1998 to date. Unfortunately, the literature remains scant on the investigation of surface water sources (tap water, raw water, surface wells, unprotected springs, lakes, rivers, and boreholes) for the possible contamination with Vibrio spp., before usage. In many low resource settings of African countries, outbreaks are contained without a regular surveillance system, leaving the populations in such hard-to-reach areas at high risk of outbreaks of waterborne diseases. As a result, no quality reports of vibriosis mortality and morbidity from such affected areas/regions. Scientific research is not encouraged, with no knowledge, technology transfer, or required resources.

Furthermore, the rank order of these countries differ when productivity is measured based on the number of TC per country, with only the United States maintaining the same positions. Similar results obtained from other parameters and other research areas in the developed, developing, and mid-economy nations such as the United States, China, Japan, India, France, Spain, Brazil, South Korean, Canada, Germany, Mexico, and Australia take the lead in productivity with insufficient research from low-income countries. It has been reported that research output influences a country’s development and its economic strength (growth).^69,94 The results also show research and economic disparity where the USA is more successful because of the budget allocation for research compared to Nigeria. This has economic and policy implications concerning research advancement in both Vibrio and other research-related policies. Therefore, policymakers should allocate funding systems motivation awards to researchers in affected countries for studies on emerging and re-emerging pathogens.

Keyword analysis provides a research advantage in discovering the path of science, and specifically, the author’s keyword gives information on current trends in a subject study.^95,96 Therefore, author’s keywords in bibliometrics analysis are recently used to analyze research trends.^31,96 Similarly, our study keywords indicate that vibriosis is ill health caused by infection with one of the several members of the genus Vibrio or related genera Photobacterium.⁹⁷ The Vibrionaceae family has changed several times due to advancements in species identification to new dynamics of family vibrionaceae using multilocus sequence analysis (MLSA) of 8 gene loci; the ftsZ, gapA, gyrB, mreB, pyrH, recA, and TopA gene sequences from 96 taxa.⁹⁸ Species frequently mentioned in the span time of this review is V. cholerae causes cholera infections. V. parahaemolyticus, is pathogenic to both humans and animals, causes gastroenteritis⁴² in humans and acute hepatopancreatic necrosis disease or AHPND, shrimp Asian countries, China, Vietnam, Thailand, and Malaysia,⁹⁹ bivalve mollusk and crustaceans, oyster, clam, and shellfish in Asia^100,101 and several European countries.¹⁰² V. vulnificus causes fatal foodborne pathogens in the United States, septicemia or wound infections.¹⁰³ V. alginolyticus, formerly regarded as biotype 2 of V. parahaemolyticus,¹⁰⁴ is an emerging threat to aquaculture as reported in Mediterranean countries, Tunisia,¹⁰⁵ Turkey,¹⁰⁶ India and Taiwan,¹⁰⁷ Spain and Israel,⁸⁶ Saudi Arabia,¹⁰⁸ Uganda.³ V. harveyi is an emerging opportunistic pathogen affecting many aquatic animals worldwide. The findings also show that Vibrio spp. is transmitted as marine bacteria that possess resistance genes, like horizontal gene transfer by which they are resistant to the current antimicrobial agents. PCR is one of the effective tools for characterization and speciation of Vibrio spp.

Geographical location appears to have impacted research collaboration because Italy collaborated most with Sweden, the USA with Mexico and Japan with India. However, the study shows more excellent research contributions and collaborations from high-income countries than low-income countries and scanty collaboration with developing countries. Authors, institutes, and countries engaged in research on the subject of Vibrio spp. have produced not more than 5 titled research contributions over the 16 years. Nevertheless, the fluctuation in research production is an index of global awareness of vibriosis outbreaks.

Limitations

This analysis quantifies and qualifies the scope and adequacy of research efforts in Vibrio spp., disciplines. However, there are limitations to this review, including the use of only 2 databases for the study. There is no doubt that significant data in other databases if included in future studies, may change the narrative of the findings of this present study. The confidence is that even under such a study beyond the scope of this review, the findings of this study will remain relevant and will serve as a pointer to important policy in this field.

Secondly, the use of titled search specificity and refined to only English Language and the exclusion of the document types (book chapter, proceedings paper, correction, letter, meeting abstract, note, review) may have limited the analysis. However, we strongly believe that having based this study on the mainstream search of the ISI WOS and Scopus databases; the excluded book chapter, proceedings paper, correction, letter, meeting abstract, note, review, when included in the future study, will have minimum impact on the findings of this study because there is a strong relationship between book chapter, proceedings paper, correction, letter, meeting abstract, note, review, and articles published in mainstream databases

Conclusion

This analysis reveals the research progress and characteristics of a 3-decade global survey on the subject of Vibrio spp. and associated diseases. We have outlined a constant average decade by decade increase in research interest regarding Vibrio and associated diseases from this review. This is because research interest doubled from the first decade to the second decade and tripled from the second to the third decade. Geopolitical location impacted research collaboration. The delineated disease distribution pattern also underscores the impact of economic status in disease control, whereby developing countries with the most significant disease burden have less capacity to control the distribution than developed countries counterparts. Increased funding of various emerging research interests irrespective of geographical locations is recommended. Finally, we recommend multifactorial bibliometric analysis to explore emerging themes and recent research focus for future directives.

Footnotes

Funding:

The author(s) received no financial support for the research, authorship, and/or publication of this article.

Declaration of Conflicting Interests:

The author(s) declared no potential conflicts of interest with respect to the research, authorship, and/or publication of this article.

Author Contributions

OH, and NUU conceived and designed the study. OH, NUU, and AE carried out the study, OH analyzed and interpreted the data, and drafted the manuscript. OH, NUU, and AE edit the manuscript. All authors read and made the final corrections.

Data Availability Statement

The datasets used for this study are available from the corresponding author on reasonable request.

ORCID iD

Hope Onohuean

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