A Bibliometric Analysis on the Association Between Pesticides and Lipoprotein

Abstract

(1) Background: The literature indicates that pesticide use and exposure can lead to neurodegenerative and carcinogenic effects in living organisms. Additionally, pesticides have been reported to influence lipid metabolism. Based on this, the objective of this analysis was to identify the most relevant authors, countries, institutions, and journals addressing the relationship between pesticides and lipoproteins; (2) Methods: The analysis was conducted using the Web of Science database and bibliometric tools, including Bibliometrix/Biblioshiny and VOSViewer software; (3) Results: A total of 72 publications from 1977 to 2014 were identified, spanning 49 sources, 3453 references, and 390 authors. The journal Pesticide Biochemistry and Physiology stood out, with seven articles and an h-index of 5. The most relevant author was Samira Salihovic. China was the top country in terms of scientific output on this topic. The United Kingdom and Spain were notable for their international collaborations. Additionally, Duk Hee Lee and Monica P. Lind were found to have the highest co-citation relationship; (4) Conclusions: This analysis highlights the relatively small number of publications on pesticides and lipoproteins between 1977 and 2024, despite growing interest in the field due to its health implications. Expanding collaborations between developed and emerging countries is essential for advancing knowledge in this critical area.

1. Introduction

Over the past few decades, direct use or indirect exposure to pesticides has been associated with numerous impacts on the ecosystem and human health. Pesticides are natural or synthetic compounds that can be classified by their mechanisms of action, chemical structure, hazards, and application [1]. These compounds are generally used to defend crops against insects, weeds, and pests, and to somehow improve crop growth [2]. According to the classification based on chemical structure, the main classes are organochlorines, organophosphates, carbamates, pyrethroids, and neonicotinoids (Figure 1).

The Food and Agriculture Organization (FAO) is a specialized agency of the United Nations, and FAOSTAT Pesticides Use provides free access data on pesticides use by country for the period 1990–2022 [3]. According to FAOSTAT data, total pesticide use in agriculture in 2022 was estimated at 3.70 million tons (Mt) of active ingredients, indicating a 4% increase compared to 2021, a 13% increase in a decade, and double since 1990. Furthermore, the Americas have been the largest users of pesticides since the mid-1990s, ahead of Asia, Europe, Africa, and Oceania. In terms of countries, Brazil was the world’s largest user of pesticides in 2022, with 801 kilotons (kt) of pesticide applications for agricultural use. This was around 70 percent higher than the second largest user, the United States of America (468 kt). Asia used 1.05 Mt of pesticides in 2022, a 1 percent decrease compared with 2021 and a 76 percent increase since 1990. In 2022, the region exported 3.5 Mt, the largest quantity of pesticides. Additionally, in Europe, pesticide use in agriculture decreased from 513 kt in 2021 to 480 kt in 2022 (−7 percent). Since 1990, the growth rate was −5 percent, with a reduction in the most recent decade of 7 percent.

In the context of human health, many compounds in use have been discovered to be potentially carcinogenic and even neurotoxic [4], but the complexity and composition of these substances leave many physiological pathways still unexplored. In addition to the previously mentioned effects, increasing attention has been drawn to the link between pesticide exposure and metabolic alterations, particularly its association with a higher risk of developing obesity [5] or other metabolic diseases.

The situation for elucidating the probable mechanisms at the biochemical, molecular, or epigenetic level is something that has been developing over the decades, due to its impact on health. Thus, there are already some mechanisms of metabolic or lipid alteration proposed in the literature.

For example, exposure to organophosphates and the increase in cholesterol and total lipid levels that are observed may be related to oxidative stress induced by reactive oxygen species and consequent interference in the permeability of the hepatocyte membrane [6]. This oxidative characteristic of pesticides, not only organophosphates but also the main classes mentioned above, leads to an increase in lipid peroxidation and antioxidant incapacity of organisms caused by the increased production of free radicals [7].

Additionally, the estrogenic behavior of the pyrethroid class can lead to changes in adiponectin, a hormone involved in the degradation of fatty acids [7]. By also inducing oxidative stress with excessive production of ROS and lipid peroxidation, pyrethroids are able to accumulate in the biological membrane and tissues, causing an oxidative insult [7,8]. The literature has also demonstrated that exposure to neonicotinoids can cause lipid accumulation and increase leptin levels; in addition, abnormal lipid metabolism is observed from neonicotinoids and their metabolites through increased leptin via AMPK-α, oxidative stress, dysfunction, disorganized structure, and disorders in amino acid metabolism [9].

Significant changes in the lipid profile such as hypertriglyceridemia, high levels of low-density lipoproteins (LDL), and a decrease in high-density lipoproteins (HDL) can lead to serious pathologies. In general, HDL is known for its beneficial role in preventing atherosclerosis by transporting excess cholesterol from tissues to the liver for excretion via bile [10]. On the other hand, high levels of LDL cholesterol are potentially harmful, as they contribute to plaque formation in the arteries, leading to reduced blood flow and an increased risk of cardiovascular diseases [11].

A study found that farmers who use pesticides have a higher risk of health outcomes involving metabolic issues than organic farmers. Although the authors clarify the limitation of the study in not proposing a causal association, pesticides can alter metabolic homeostasis, disrupting appetite controls, promoting adipocytic hypertrophy, or even stimulating adipogenic pathways [12].

Furthermore, another study reported findings regarding non-occupational pesticide exposure and that all exposures (overall pesticide exposure, exposure in months, exposure in years, and specific pesticides) were positively associated with total and LDL cholesterol in women [13]. This is corroborated in the literature, showing that exposure to pesticides is associated with higher concentrations of lipids, resulting from a reduction in antioxidant enzymes and an increase in lipid peroxidation.

Considering the potential changes in the lipid profile, particularly in lipoproteins, that may be triggered by pesticide exposure, this study employed bibliometric analysis to explore and describe the body of literature examining the association between pesticides and changes in lipid metabolism and identify possible gaps in scientific production.

To date, no bibliometric analysis has systematically examined the literature linking pesticides and lipoproteins. By filling this gap, our study not only highlights the current landscape of this emerging intersection between environmental exposure and metabolic health but also provides a strategic tool for researchers and policymakers to identify knowledge gaps, high-impact authors, and collaborative opportunities. Our aim is to offer a macro-level view of the field that can guide more targeted and mechanistic research efforts in the future.

2. Materials and Methods

2.1. Database Collection, Search Strategy, and Screening Process

This research utilized the Web of Science (WoS), a multidisciplinary database that indexes the most frequently cited journals across various fields. WoS is also one of the most widely used platforms for conducting bibliometric analyses. The initial data collection took place in August 2024, using the keywords “pesticide” and “lipoprotein”. To maximize the number of results, the search was conducted across “all fields” for both terms. Filters were applied to limit the results to articles and review articles, and only the language filter was modified (

Table 1. Search strategy.

Filters	Criteria Used
Keywords	Pesticide (All Fields) and lipoprotein (All Fields)
Document types	Article and review article
Language	English

). In the subsequent phase, the dataset was refined by reviewing the titles and key topics mentioned in the abstracts of the articles.

The primary inclusion criterion was the mention of any pesticide linked to changes in any lipoprotein in the article’s abstract. The main exclusion criterion was the omission of pesticides and their association with lipoproteins as the central focus of the study.

2.2. Bibliometric Methods and Purpose of the Analysis

After exporting the information from the database, the following analysis was carried out using Bibliometrix (version 4.3.0). Bibliometrix is an open-source tool developed by Massimo Aria and Corrado Caccurullo in the statistical computing and graphic R language (version 4.2.3) [14]. It was chosen for this analysis because it encompasses all the key bibliometric analysis methods. To guide the research, the following questions were formulated, which will be addressed and discussed in the Conclusions section of this article:

• Who are the most relevant authors, countries, institutions, and journals on pesticides and lipoproteins;
• What are the most common words and keywords about pesticides and lipoproteins;
• What are the results on collaborations between countries on pesticides and lipoproteins;
• Is there a lack of research on pesticides and lipoproteins?

2.2.1. Source’s Relevance and Impact

In the evaluation of sources, the number of articles published by each source was used to rank its relevance in terms of the top ten, while the h-index assessed the impact of each source. The h-index is based on the most frequently cited articles of a source or author and the number of citations these articles have received in other publications.

2.2.2. Author’s Impact, Affiliations, and Countries

The ten most relevant authors were identified based on the number of articles published. To measure the productivity and impact of an author’s citations, the h-index was used as a metric. It measures the productivity and citation impact of a scientist’s publications. The author’s h-index obtained in this bibliometric analysis refers to this specific collection of articles included in our study. Another important factor for evaluation was the authors’ affiliations, leading to the identification of the top ten institutions based on the number of articles. Finally, the scientific production by country was analyzed; this metric counts the appearances of authors by country affiliation, meaning that in collaborative publications involving multiple countries, the count increases by one for each participating country.

2.2.3. Conceptual, Intellectual, and Social Structure

In the analysis of the conceptual structure, a network map with the co-occurrences of keywords was obtained through the VOSviewer software (version 1.6.20). The unit of analysis was “all the keywords”. This analysis is determined by the association between items and the number of documents in which they occur together.

The minimum number of occurrences of the keywords was set at six. To assess the intellectual structure, a co-citation network map was explored using VOSviewer. In this case, the analysis is determined based on the number of times the references are cited together. Therefore, the unit of analysis was “cited references”. The minimum number of citations used for a cited reference was six. The larger the number of publications by which two publications are co-cited, the stronger the co-citation relationship between the two publications. Ultimately, in the analysis of the social structure, a world map of collaborations between countries was examined.

The selected bibliometric visualizations and metrics, such as co-citation networks and keyword clustering, were chosen to provide a comprehensive overview of the field’s conceptual, intellectual, and social structure. These tools are widely adopted in strategic mapping studies, enabling us to highlight relevant actors, themes, and collaboration patterns that are otherwise difficult to observe through traditional reviews.

3. Results

In the initial search using the keywords “pesticides” and “lipoproteins” in the WoS database, 235 articles were identified. After applying filters for language and publication type, the total was reduced to 227. Subsequently, the titles and abstracts of these articles were analyzed, resulting in the exclusion of 155 articles based solely on their subject matter. This entire process is summarized in Figure 2.

Publications were retrieved spanning from 1977 to 2024, resulting in a total of 49 sources, 3453 references, and 390 authors across 72 documents. Of these, 69 were articles and 3 were review articles. This summarized information is presented in

Table 2. Main general information of the articles.

General Information	Numbers
Timespan	1977–2024
Sources (n)	49
References (n)	3453
Authors (n)	390
Document type (n)	72
Articles	69
Review articles	3

.

The software ranked the top 10 most relevant sources based on the number of articles and h-index, as shown in

Table 3. Most relevant sources and their h-index.

Sources	Articles (n)	h-Index
Pesticide Biochemistry and Physiology	7	5
Environment International	6	5
Environmental Science and Pollution Research	6	5
Environmental Research	4	4
Chemosphere	2	2
Ecotoxicology and Environmental Safety	2	2
Human & Experimental Toxicology	2	2
International Journal of Environmental Research and Public Health	2	2
Acta Medica Scandinavica	1	1
American Journal of Hypertension	1	1

.

The standout source was Pesticide Biochemistry and Physiology, which published seven articles and has an h-index of 5. Following closely were Environment International and Environmental Science and Pollution Research, each with six articles and an h-index of 5. Additionally, Environmental Research contributed four articles to the analysis. The following sources each published two articles: Chemosphere, Ecotoxicology and Environmental Safety, Human & Experimental Toxicology, and International Journal of Environmental Research and Public Health. Finally, American Journal of Hypertension and Acta Medica Scandinavica each contributed one article. Next, we analyzed the ten most relevant authors, as detailed in

Table 4. Most relevant authors.

Sources	Articles (n)
Salihovic, Samira	4
Jin, Yuanxiang	3
Kongtip, Pornpimol	3
Lind, Lars	3
Lind, P. Monica	3
Nankong, Noppanun	3
Van Bavel, Bert	3
Woskie, Susan	3
Abass, Khaled	2
Aminov, Zafar	2

.

The most prominent author was Samira Salihovic, who published four articles. Following Samira Salihovic, the next authors were Yuanxiang Jin, Pornpimol Kongtip, Lars Lind, Monica P. Lind, Noppanun Nankongnab, Bert Van Bavel, and Susan Woskie, each with three articles. Lastly, Khaled Abass and Zafar Aminov each contributed two articles to the list.

Similarly, the local impact of the authors, that is, considering only the 72 documents included in this analysis, was assessed based on the h-index and total number of citations (

Table 5. Author’s local impact.

Sources	h-Index	Total Citation
Salihovic, Samira	4	185
Kongtip, Pornpimol	3	45
Lind, Lars	3	126
Lind, P. Monica	3	126
Nankong, Noppanun	3	45
Van Bavel, Bert	3	177
Woskie, Susan	3	45
Aminov, Zafar	2	73
Ben Amara Ibtissem	2	33
Bombidick, D. W.	2	71

).

That said, the indices ranged from 2 to 4, since the analysis only involved articles that discussed pesticides and lipoproteins. Samira Salihovic stood out, with an h-index of 4 and a total of 185 citations. Pornpimol Kongtip followed with an h-index of 3 and 45 citations. Both Lars Lind and Monica P. Lind also had an h-index of 3, with each author receiving 126 citations.

They were followed by Noppanun Nankongnab, Bert Van Bavel, and Susan Woskie, each with an h-index of 3 and citations of 45, 177, and 45, respectively. Finally, Zafar Aminov, Ibtissem Ben Amara, and David W. Bombick all had an h-index of 2, with 73, 33, and 71 citations, respectively. We also examined the ten most relevant affiliations (

Table 6. Most relevant affiliations ranked.

Affiliations	Articles (n)
Chinese Academy of Sciences	9
Universite de Sfax	8
University of Oulu	8
China Agricultural University	6
Tehran University of Medical Sciences	6
Universitat Rovira i Virgili	6
Uppsala University	6
Egyptian Knowledge Bank (EKB)	5
Imperial College London	5
Mahidol University	5

).

The Chinese Academy of Sciences led with nine articles, followed by the University of Sfax and the University of Oulu, each with eight articles. Next, China Agricultural University, Tehran University of Medical Sciences, Universitat Rovira i Virgili, and Uppsala University each contributed six articles. Finally, the Egyptian Knowledge Bank (EKB), Imperial College London, and Mahidol University each published five articles.

Figure 3 illustrates the evaluation of scientific production by country, highlighting the five countries with the highest outputs. China had the largest representation, with a total of 44 publications. Following China, the United States contributed 29 articles, while Spain, Iran, and Sweden had 27, 24, and 19 publications, respectively.

Next, a co-occurrence map of keywords was created. Out of 554 keywords identified, 21 met the threshold of appearing at least six times. The resulting visualization is presented in Figure 4, which reveals three distinct clusters represented in red, green, and blue. Notably, the word “pesticide” appeared 19 times, “oxidative stress” 18 times, and “toxicity” 17 times, all within the red cluster. In the blue cluster, the keyword “exposure” occurred 17 times. Lastly, within the green cluster, the term “persistent organic pollutant” was highlighted, appearing 10 times.

As mentioned earlier, a higher number of citations appearing together in a publication indicates a stronger co-citation relationship between the two documents. Notably, Duk Hee Lee and Monica P. Lind exhibited the highest co-citation relationship in this analysis.

The countries with the highest number of international collaborations were the United Kingdom and Spain (Figure 5). The UK accounted for 16 collaborations, including 3 with Norway and 2 with Finland, and the remaining collaborations were with various other countries.

Spain also had 16 collaborations, and of these, 4 were with the United Kingdom, 3 with Norway, and 2 with Finland. The remaining collaborations were individual collaborations with different countries. In addition to these, 13 collaborations originated from the United States, of which 3 were with Thailand. It also collaborated once with the United Kingdom, once with Norway, and once with Spain. Finally, eight collaborations originated from Norway in total, and these were all with different countries.

4. Discussion

Bibliometric analysis is a valuable technique for mapping the intellectual landscape of a research field and assessing its evolution, as well as the interrelationships among authors, topics, and articles [9]. The utilization of specialized software is crucial in bibliometrics, given the variety of tools available today [10].

Because we were interested in screening the subject of pesticides and lipoproteins, we performed a bibliometric analysis with the purpose of collecting and analyzing basic information, such as the number of documents, data on the authors and timeline, and also more specific information about the imported documents, such as clusters of co-occurrences of keywords. During the data analysis process, the bibliometric analysis became a starting point to gain information for more specific research in the future.

In our descriptive analysis of data extracted from the Web of Science database, we identified 72 articles published between 1977 and 2024, authored by 390 individuals across 49 different sources. Notably, we found a scarcity of literature reviews addressing the relationship between pesticides and lipoproteins, with only 3 relevant documents identified from the 72 analyzed.

Despite the limited number of publications over 49 years, there is a growing interest in understanding the metabolic changes induced by pesticides, particularly in relation to diseases of significant epidemiological concern, such as obesity and cardiovascular disease (CVD).

A study identified an association between p,p’-DDE exposure and altered lipid levels in a large human cohort, suggesting it could be an unrecognized risk factor for cardiovascular disease (CVD) [15]. Another investigation found that non-occupational pesticide exposures were linked to decreased HDL concentrations across all lipoprotein subclasses [16]. These findings underscore the need for further research to address the significant gaps in understanding the mechanisms and pathways through which pesticides induce metabolic alterations.

Samira Salihovic emerged as the most prominent author in terms of relevance and impact, currently affiliated with Örebro University in Sweden. She contributed four articles, which garnered the highest number of citations—185 in total. In terms of global scientific output, China is particularly notable, with 44 published articles, although it has not demonstrated significant international collaborations in this area. This trend is reflected in the affiliations leading this analysis, particularly the Chinese Academy of Sciences and China Agricultural University, which collectively accounted for 15 publications.

When analyzing the three clusters obtained from the co-occurrences of keywords, it was possible to investigate some of the terms individually that stood out among the clusters.

In the blue cluster, the term “exposure” appeared most frequently (17 times). We were able to observe that the theme of “lipid profile” has a connection with the class of organophosphates, more specifically, the pesticides that appeared were chlorpyrifos and diazinon. Thus, we found a recent study which showed that the exposure of chlorpyrifos altered the lipid profile in albino rats, leading to increased low-density lipoprotein (LDL) levels and decreased high-density lipoprotein (HDL) levels in serum [17].

Furthermore, in the green cluster, the keyword “persistent organic pollutant” stood out alongside the class of polychlorinated biphenyls, having associations with terms involving physiological disorders such as cardiovascular disease and insulin resistance.

Finally, the red cluster was more involved with the toxicity mechanisms caused by pesticides, such as oxidative stress and lipid peroxidation.

Following China, the United States ranks next with 29 articles, along with 13 collaborations with other countries, including Thailand, the United Kingdom, Sweden, and Spain. Spain also stands out, with 27 publications, notably featuring Universitat Rovira i Virgili in Catalonia, which ranks among the most relevant affiliations with six articles. The UK and Spain were the most collaborative, each engaging in 16 partnerships, including with Norway and Finland. This pattern highlights a strong level of collaboration and prominence among “First World” countries.

In addition to the highlighted aspect of the lack of collaboration with so-called “developing countries”, we can point out that some of these countries are large users of pesticides [3] and their exposed populations are said to be unique both in terms of exposure and genetic characteristics [18].

That said, it is of great interest to promote publications and research with these countries, which have a favorable situation for analysis and possible new discoveries related to this topic.

In terms of co-citation, authors Duk Hee Lee and Monica P. Lind have the highest relationship, as previously mentioned. Lind’s research focuses on the effects of exposure to environmental endocrine-disrupting chemicals and she is affiliated with Uppsala University, which ranks highly in relevance, with six publications.

As with all bibliometric analyses, the results of this study represent the state of the literature up to the date of data extraction. Given the dynamic nature of scientific production, future updates will be necessary to incorporate new studies and shifting trends. Nonetheless, the long time span covered (1977–2024) provides a robust foundation for identifying historical patterns and emerging themes.

5. Conclusions

The study of the impact of pesticide exposure on living organisms is well established in the literature, particularly concerning neurodegenerative diseases and cancers. However, due to the complexity of these substances, many mechanisms remain unknown, and several topics are not thoroughly understood. This bibliographic analysis specifically focuses on the association between pesticides and their effects on lipoproteins—an area that currently lacks sufficient publications, despite a growing interest in the metabolic harm caused by pesticide exposure. Our findings indicate a limited number of studies, with most originating from well-developed countries. There is a pressing public interest and an epidemiological imperative for further investigations into this topic. The macroscopic analysis provided by the bibliometrics of pesticides and lipoproteins became a starting point for building a strong theoretical framework for possible future work related to this topic. This analysis highlights the need not only for further mechanistic studies but also for more inclusive, globally collaborative research to understand how pesticide exposure differentially affects metabolic health across diverse populations.