Global research production in glyphosate intoxication from 1978 to 2015: A bibliometric analysis

Abstract

Background:

Glyphosate (N-phosphonomethylglycine) has been used as a broad-spectrum herbicide that has been widely used in the agricultural industry and also available for home use. The main aim of this study is to present a general overview of glyphosate intoxication-related publications from its introducing since the early 1970s using bibliometric technique.

Methods:

On June 23, 2016, a literature search of the Scopus database was performed. We then extracted and analyzed the data using well-established qualitative and quantitative bibliometric indices: Publication year, affiliation, document type, country name, subject category, journal name, publishing language, and collaboration and citation patterns.

Results:

We recognized a total of 3735 publications on glyphosate published between 1973 and 2015. There were 875 publications related to glyphosate intoxication in the Scopus database published between 1978 and 2015. Articles (757) comprised 86.5% of the total publications, followed by reviews (41; 4.7%). Most publications were published in English (87.9%), followed by Portuguese (6.6%). The number of publications related to glyphosate intoxication increased from 44 in 1978–1987 up to 152 in 1996–2005 and then quadrupled in 2006–2015. The United States was the leading country with 180 documents representing 20.6%, followed by Brazil (120; 13.7%), Canada (78; 8.9%), Argentina (61; 7.0%), and France (57; 6.5%). The 85.6% of the publications was cited, and the average of citation per document was 17.13 with h-index of 55. Furthermore, the United States achieved the highest h-index of 33. Most of the global international collaborations are made with researchers from the United States, who collaborated with 23 countries/territories in 44 publications.

Conclusions:

The trends in global glyphosate-related research between 1978 and 2015 were evaluated by a bibliometric technique. Results showed that English was the leading publishing language, and the major publication type was original article. Findings showed that number of research publications related to glyphosate intoxication increased significantly in the last decade. The United States and Brazil are the two most productive countries in research on glyphosate intoxication. This study will be beneficial to policy makers by identifying areas that need greater investment and research funding to target appropriate agriculture sectors so as to improve glyphosate safety in a global setting.

Keywords

Glyphosate poisoning bibliometric Scopus

Introduction

Glyphosate (N-phosphonomethylglycine) has been used as a broad-spectrum herbicide that has been available since the early 1970s. It is widely used in the agricultural industry and also available for home use.¹ Glyphosate is the active constituent of many different proprietary herbicide preparations and is typically accompanied by the presence of a surfactant agent such as polyethoxylated tallow amine. Glyphosate is absorbed through plant foliage and is active against a variety of weeds and grasses.^2,3 Its mechanism of action is inhibition of 5-enolpyruvoylshikimate-3-phosphate synthase (EPSPS), which catalyzes the formation of aromatic amino acid in plants, namely tyrosine, tryptophan, and phenylalanine, and secondary metabolites including tetrahydrofolate, ubiquinone, and vitamin K. The EPSPS pathway is absent in humans, other mammals, fish, birds, and insects so that its action is selective for plants. Moreover, several glyphosate-resistant crops have been developed, so that its activity is made even more specific to weeds.^2,4

The global use of glyphosate is growing, and there is evidence for persistence of glyphosate in food and water supplies as a source of human exposure.⁵ There is little oral absorption of glyphosate or its key metabolite aminomethylphosphonic acid and neither is subject to bioaccumulation. There are no significant biochemical or physiological effects observed in acute, subchronic, and chronic glyphosate administration studies in animals involving much higher doses that would be anticipated with environmental exposures, and no known irritant or carcinogenic effects. A comprehensive safety evaluation and risk assessment of a large body of data have concluded that the herbicidal use of glyphosate poses no risk to human health.⁶ Despite some controversial findings that have suggested possible human health effects, a number of epidemiological studies have failed to identify any link between glyphosate exposure and the occurrence of human cancer, and there have been no proven developmental or reproductive health effects.^7,8 Recently, the International Agency for Research on Cancer considered glyphosate as category 2A, which is probably carcinogenic in humans based on several epidemiological studies on human, in vitro studies, and animal studies.⁹

In contrast to the use of glyphosate as a herbicide, intentional human exposures may cause significant toxic effects, particularly after ingestion of concentrated preparations intended for professional use or exposures involving the intravenous route of administration. Toxic clinical features are likely to be attributable to the surfactant component of the herbicide formulation, rather than glyphosate itself. These may include gastrointestinal symptoms, tachypnea, pulmonary edema, hypotension, rhabdomyolysis, renal failure, hemolysis, and coma. Fatalities occur in around 2–3% of patients who have ingested large quantities of highly concentrated glyphosate formulations, typically involving more than 75 mL of at least 10% concentration.¹⁰ Hyperkalemia is a recognized complication, especially after ingestion of formulations that contain glyphosate potassium salt.¹¹ Treatment is supportive to maintain a clear airway, adequate ventilation and circulation, and close monitoring of the electrocardiograph and serum electrolytes. Gastric lavage may be considered within 1 h of ingesting a large, life-threatening quantity of concentrated glyphosate formulation, although evidence of improved outcome is lacking. Patients with hypotension or cardiac arrhythmia should normally be managed in a critical care setting, including careful monitoring of fluid balance and acid-base status, and administration of vasopressors and positive inotropes.^10,12 Intravenous lipid administration may be effective in some patients with severe glyphosate cardiotoxicity.¹³ Hemodialysis or hemofiltration may be required if patients develop hyperkalemia or acute renal failure.¹⁴

However, no study has been published presenting a general overview of glyphosate research. Some researchers have studied some specific aspects in toxicology field using the bibliometric techniques, including paracetamol poisoning,¹⁵ intravenous lipid emulsion as an antidote,¹⁶ N-acetylcysteine use in paracetamol overdose,¹⁷ methanol poisoning,¹⁸ and calcium channel blockers poisoning.¹⁹ The main aim of this study is to present a general overview of glyphosate intoxication-related publications from its introducing since the early 1970s using bibliometric technique. Analysis of such data gives us insight into how our understanding about glyphosate intoxication has developed.

Methods

On June 23, 2016, a literature search of the Scopus database was performed. Key search words included glyphosate OR N-phosphonomethylglycine OR Roundup* were used as keywords to search all publications that contained these terms in the title. Then, to extract only publications related to glyphosate intoxication, the following keywords: *toxic* or poison* (an asterisk replaces any number of characters) in the title, abstract, or keywords list. The methodology used in the current study was similar to several studies in the field of bibliometric from our research group.^{15

–23} In this approach, it was possible to get the publications published in the period comprised between 1978 (first documents in the field glyphosate intoxication²⁴) and 2015. We excluded all 2016 publications from our analysis because this year stills open for new issues from the indexed journals.

We then extracted and analyzed the data using well-established qualitative and quantitative bibliometric indices: Publication year, affiliation, document type, country name, subject category, journal name, publishing language, and collaboration and citation patterns. In the current study, two indicators of influence are used, that is, the impact factor (IF) that was extracted from the Journal Citation Reports 2015 published in 2016 and the h-index.

Statistical analysis

The data were downloaded into a Microsoft Excel spreadsheet for analysis. Statistical analyses were carried out using the SPSS 15.0 statistical package to get frequency and percentage.

Results

We recognized a total of 3735 publications on glyphosate published between 1973 and 2015. There were 875 publications related to glyphosate intoxication in the Scopus database published between 1978 and 2015. Articles (757) comprised 86.5% of the total publications, followed by reviews (41; 4.7%), letters (23; 2.6%), and conference papers (17; 1.9%). Other document types such as notes, editorial materials, or book reviews covered around 4.2% of the published literature. Fifty-four (7.1%) publications were case reports or case series. As shown in Figure 1, the number of publications related to glyphosate intoxication increased from 44 in 1978–1987 up to 152 in 1996–2005 and then quadrupled in 2006–2015. The selected publications were published in 17 different languages. Most publications were published in English (87.9%), followed by Portuguese (6.6%), and Spanish (1.3%).

Figure 1.

The publication output performance of glyphosate intoxication documents.

Table 1 presents the top 10 countries/territories with regard to the number of total publications with their h-index and collaboration patterns. Table 1 demonstrates that the United States was the leading country with 180 documents representing 20.6%, followed by Brazil (120; 13.7%), Canada (78; 8.9%), Argentina (61; 7.0%), and France (57; 6.5%). The 85.6% of the publications was cited, and the average of citation per document was 17.13 with h-index of 55. Furthermore, the United States achieved the highest h-index of 33, followed by Brazil and Canada with h-index of 23 for each one. Most of the global international collaborations are made with researchers from the United States, who collaborated with 23 countries/territories in 44 publications, followed by researchers from France who collaborated with 16 countries/territories in 18 publications (Table 1).

Table 1.

Top 10 most productive countries/territories in research on glyphosate intoxication field.

SCR^a	Country	Number of documents (%)	h-index	Number of collaborate countries	Number of publications from collaboration (%)
1st	United States	180 (20.6)	33	23	44 (24.4)
2nd	Brazil	120 (13.7)	23	9	8 (6.7)
3rd	Canada	78 (8.9)	23	14	21 (26.9)
4th	Argentina	61 (7.0)	19	3	4 (6.6)
5th	France	57 (6.5)	20	16	18 (31.6)
6th	United Kingdom	33 (3.8)	14	14	20 (60.6)
7th	China	25 (2.9)	8	3	7 (28.0)
8th	Italy	24 (2.7)	12	14	13 (54.2)
9th	Germany	23 (2.6)	13	10	12 (52.2)
9th	India	23 (2.6)	5	3	4 (17)

SCR: standard competition ranking.

^aEqual countries have the same ranking number, and then a gap is left in the ranking numbers.

The top 10 most productive journals are summarize in Table 2, along with IF of each journal. More than 31% of the glyphosate intoxication-related publications are published in the top 10 journals listed in Table 2. Bulletin of Environmental Contamination and Toxicology is the most productive journal with 56 documents, followed by Planta Daninha with 39 documents, Environmental Toxicology and Chemistry with 33 documents, and Ecotoxicology and Environmental Safety with 27 documents. Table 3 shows the top 10 research areas. The Scopus contains 396 publications in Environmental Science, followed by 297 publications in Pharmacology, Toxicology and Pharmaceutics, 272 publications in Agricultural and Biological Sciences, and 194 publications in Medicine (Table 3).

Table 2.

The 10 most productive journals.

SCR^a	Journal	Frequency (%)	IF
1st	Bulletin of Environmental Contamination and Toxicology	56 (6.4)	1.191
2nd	Planta Daninha	39 (4.5)	0.395
3rd	Environmental Toxicology and Chemistry	33 (3.8)	2.763
4th	Ecotoxicology and Environmental Safety	27 (3.1)	3.13
5th	Chemosphere	22 (2.5)	3.698
6th	Archives of Environmental Contamination and Toxicology	21 (2.4)	2.039
7th	Pesticide Biochemistry and Physiology	17 (1.9)	2.388
8th	Clinical Toxicology	16 (1.8)	2.886
9th	Aquatic Toxicology	15 (1.7)	3.557
9th	Environmental Toxicology and Pharmacology	15 (1.7)	2.187
9th	Food and Chemical Toxicology	15 (1.7)	3.584

SCR: standard competition ranking.

^aEqual journals have the same ranking number, and then a gap is left in the ranking numbers.

Table 3.

The top 10 most subject categories related to glyphosate intoxication.

SCR	Subject category	Frequency (%)
1st	Environmental Science	396 (45.3)
2nd	Pharmacology, Toxicology and Pharmaceutics	297 (33.9)
3rd	Agricultural and Biological Sciences	272 (31.1)
4th	Medicine	194 (22.2)
5th	Biochemistry, Genetics and Molecular Biology	126 (14.4)
6th	Chemistry	48 (5.5)
7th	Earth and Planetary Sciences	30 (3.4)
8th	Immunology and Microbiology	21 (2.4)
9th	Veterinary	16 (1.8)
10th	Chemical Engineering	12 (1.4)

SCR: standard competition ranking.

The top 20 most cited publications related to glyphosate intoxication are shown in Table 4.^4,6,25–42 Obviously, the paper by Giesy et al.²⁵ in 2000 is the most influential and cited one with 365 citations, followed by paper for Duke and Powles⁴ with 327 citations. Table 5 presents a list of the 10 most influential institutions in glyphosate intoxication-related research. The Monsanto Company from the United States had the most contribution with 31 publications, followed by the Universidade Federal de Vicosa in Brazil with 26 publications.

Table 4.

The top 20 most cited publications related to glyphosate intoxication.^{4,6,25

–42}

SCR^a	Authors	Title	Year of publication	Source title	Cited by	Article type
1st	Giesy et al.²⁵	“Ecotoxicological Risk Assessment for Roundup^® Herbicide”	2000	Reviews of Environmental Contamination and Toxicology	365	Review
2nd	Duke and Powles⁴	“Glyphosate: A Once-in-a-Century Herbicide”	2008	Pest Management Science	327	Review
3rd	Williams et al.⁶	“Safety Evaluation and Risk Assessment of the Herbicide Roundup and Its Active Ingredient, Glyphosate, for Humans”	2000	Regulatory Toxicology and Pharmacology	286	Review
4th	Tsui and Chu²⁷	“Aquatic Toxicity of Glyphosate-Based Formulations: Comparison Between Different Organisms and the Effects of Environmental Factors”	2003	Chemosphere	205	Original
5th	Howe et al.²⁶	“Toxicity of Glyphosate-Based Pesticides to Four North American Frog Species”	2004	Environmental Toxicology and Chemistry	168	Original
6th	Richard et al.²⁸	“Differential Effects of Glyphosate and Roundup on Human Placental Cells and Aromatase”	2005	Environmental Health Perspectives	167	Original
7th	Relyea²⁹	“The Lethal Impact of Roundup on Aquatic and Terrestrial Amphibians”	2005	Ecological Applications	165	Original
7th	Walsh et al.³⁰	“Roundup Inhibits Steroidogenesis by Disrupting Steroidogenic Acute Regulatory (StAR) Protein Expression”	2000	Environmental Health Perspectives	165	Original
9th	Mann and Bidwell³¹	“The Toxicity of Glyphosate and Several Glyphosate Formulations to Four Species of Southwestern Australian Frogs”	1999	Archives of Environmental Contamination and Toxicology	163	Original
10th	Busse et al.³²	“Glyphosate Toxicity and the Effects of Long-Term Vegetation Control on Soil Microbial Communities”	2001	Soil Biology and Biochemistry	151	Original
11th	Folmar et al.³³	“Toxicity of the Herbicide Glyphosate and Several of Its Formulations to Fish and Aquatic Invertebrates”	1979	Archives of Environmental Contamination and Toxicology	143	Original
12th	Relyea³⁴	“The Lethal Impacts of Roundup and Predatory Stress on Six Species of North American Tadpoles”	2005	Archives of Environmental Contamination and Toxicology	140	Original
13th	Malik et al.³⁵	“The Herbicide Glyphosate”	1989	BioFactors	131	Review
14th	Benachour and Séralini³⁶	“Glyphosate Formulations Induce Apoptosis and Necrosis in Human Umbilical, Embryonic, and Placental Cells”	2009	Chemical Research in Toxicology	124	Original
15th	Gasnier et al.³⁷	“Glyphosate-Based Herbicides Are Toxic and Endocrine Disruptors in Human Cell Lines”	2009	Toxicology	122	Original
16th	Harrison et al.³⁸	“The Expressed Protein in Glyphosate-Tolerant Soybean, 5-Enolypyruvylshikimate-3-Phosphate Synthase from Agrobacterium sp. Strain CP4, Is Rapidly Digested In Vitro and Is Not Toxic to Acutely Gavaged Mice”	1996	Journal of Nutrition	120	Original
17th	Cavaş and Könen³⁹	“Detection of Cytogenetic and DNA Damage in Peripheral Erythrocytes of Goldfish (Carassius auratus) Exposed to a Glyphosate Formulation Using the Micronucleus Test and the Comet Assay”	2007	Mutagenesis	119	Original
18th	Séralini et al.⁴⁰	“Long Term Toxicity of a Roundup Herbicide and a Roundup-Tolerant Genetically Modified Maize”	2012	Food and Chemical Toxicology	112	Original
19th	Modesto and Martinez⁴¹	“Roundup^® Causes Oxidative Stress in Liver and Inhibits Acetylcholinesterase in Muscle and Brain of the fish Prochilodus lineatus”	2010	Chemosphere	106	Original
19th	Glusczak et al.⁴²	“Acute Effects of Glyphosate Herbicide on Metabolic and Enzymatic Parameters of Silver Catfish (Rhamdia quelen)”	2007	Comparative Biochemistry and Physiology—C Toxicology and Pharmacology	106	Original

SCR: standard competition ranking.

^aEqual articles’ citation have the same ranking number, and then a gap is left in the ranking numbers.

Table 5.

The top 10 most productive institutes.

SCR^a	Institute	Country	n (%)
1st	Monsanto Company	United States	31 (3.5)
2nd	Universidade Federal de Vicosa	Brazil	26 (3.0)
3rd	Universidade Estadual Paulista (UNESP)	Brazil	23 (2.6)
4th	Universite de Caen Basse Normandie	France	21 (2.4)
5th	Universidad de Buenos Aires	Argentina	18 (2.1)
6th	University of Guelph	Canada	14 (1.6)
7th	Consejo Nacional de Investigaciones Cientificas y Tecnicas	Argentina	13 (1.5)
8th	University of Ibadan	Nigeria	12 (1.4)
8th	Universidade de Sao Paulo (USP)	Brazil	12 (1.4)
8th	Universidad Nacional del Litoral	Argentina	12 (1.4)

SCR: standard competition ranking.

^aEqual institutes have the same ranking number, and then a gap is left in the ranking numbers.

Discussion

The current study is the first quantitative bibliometric analysis of glyphosate intoxications in the field of toxicology and the findings indicated that the total growth of the glyphosate literature is apparently rapid in the last decade. This might be due to the current “publish or perish” climate, or the widespread use of Internet, which has allowed faster spreading of medical knowledge,⁴³ but also due to the increasing interest in assessment of glyphosate safety. The majority of worldwide publications on glyphosate research appeared after 2000. The increase in research output at global level on glyphosate might related to the increasing worldwide glyphosate morbidity and mortality which are increasing along with the growing prevalence of glyphosate usage,^{12,14,44

–49} or due to an emerging issue which demonstrated a correlations between exposure to glyphosate and cancer manifested as an increase in the number of research in this field.^{1,5,50

–54}

The United States was seen to be the largest contributor in the field of glyphosate, a finding that agrees with previous similar bibliometric studies in different fields in toxicology.^{15

–19,55} This research activity from the United States is likely due to the economic strength, or nation’s large size,^56,57 or numerous large poison centers.⁵⁸ Furthermore, Brazil leadership in glyphosate global research obviously stands up, most probable due to the fact that it was in this country where considered as one of the top five users worldwide for pesticides, accounted for 40% of total consumption in Latin America.^59,60

In our study, English language publications were the most common, possibly due to the fact that the United States was the largest contributor to glyphosate literature. Furthermore, Scopus is a US-based database, and English is considered the official language for most international journals.⁶¹

Some of the findings are similar to those found in previous bibliometric studies in other fields, mainly the fact that the United States dominates the international collaboration, also has the highest h-index.^{15,16,18

–22,62,63} International collaboration in research is desired to address priorities in creating new ideas in this field and to fund research,⁶⁴ in addition, international collaboration allows researchers to contribute in multicenter clinical trials and enhances the quality of the research by a positive effect on citation rates.⁶⁵ In the current study, the average number of citations per article was 17.13, which is higher than the number of citations for articles in the general field of toxicology.^{15,16,18
–20,66
–68} This finding suggests that glyphosate intoxication has a large audience in scientific research and still an area of active research in toxicology. This finding is also possibly due to fact that glyphosate intoxication is a multidisciplinary field, as shown in the broad range of subject categories of publications. In addition to Pharmacology, Toxicology and Pharmaceutics category, we found that Environmental Science and Agricultural and Biological Sciences were most common research subjects.

The top cited articles in the list of the most cited publications on glyphosate intoxication were “review articles.”^4,6,25 Review articles are generally cited more than original research articles.^69
–71 The reason behind this is that structural features of review articles such as the number of pages and references would be higher in review articles than in original ones.³ Another possible explanation for this is that the number of co-authors and institutional collaboration would be higher in review studies, which increases the possibility of so many co-authors to cite the review articles.⁶⁹

However, this study is the first attempt to evaluate trends in global glyphosate-related research, the main limitation with this bibliometric analysis lies that the literature search was relied on a single database. Scopus database was selected because it is the largest database,⁷² and majority of researchers in the field of bibliometrics have been widely used it in similar studies.^{16,21,22,73

–77}

Conclusions

The trends in global glyphosate-related research between 1978 and 2015 were evaluated by a bibliometric technique. Results showed that English was the leading publishing language, and the major publication type was original article. Findings showed that number of research publications related to glyphosate intoxication increased significantly in the last decade. Environmental Science and Pharmacology, Toxicology and Pharmaceutics were the top two most central subject categories. Bulletin of Environmental Contamination and Toxicology is the most productive journal. The United States and Brazil are the two most productive countries in research on glyphosate intoxication. This study will be beneficial to policy makers by identifying areas that need greater investment and research funding to target appropriate agriculture sectors so as to improve glyphosate safety in a global setting.

Footnotes

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.

Funding

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

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