A scientometric study of syphilis research by dermatologists and stomatologists: Underpinning their roles in public health
Syphilis is a sexually and vertically transmitted bacterial infection caused by the bacterium T pallidum . The prevalence of syphilis is high in low income and middle income countries, and it is a major cause of adverse pregnancy outcomes in these countries. High income countries have had a low prevalence of syphilis among heterosexual men and women, but a resurgence of the infection has occurred among men who have sex with men (MSM), in the last few decades. In Europe, an increased incidence of syphilis has been reported since 2010. This trend appears to be accelerating, especially among MSM. Syphilis has increased by 80% in the United States over the past 5 years, as reported by the US Centers for Disease Control and Prevention. Outbreaks in heterosexual populations have also been reported, with an increase in congenital syphilis cases. Moreover, patients with syphilis present a higher risk of being infected by other sexually transmitted diseases (STDs), especially acquired immunodeficiency syndrome caused by human immunodeficiency virus (HIV), because syphilitic lesions are vulnerable sites for virus penetration. Syphilis has long been a menacing human pathogen and remains a pertinent global public health concern. The course of syphilis is separated into three stages: primary, secondary, and tertiary; lesions can present in a variety of ways depending on the stage. Dermatologists are uniquely positioned to identify the disease in incipient stages, given its prominent cutaneous manifestations, thus steering prompt treatment, preventing complications, and interrupting the chain of transmission. Opportunistic testing in dermatology clinics, where patients seek services that include genital wart removal, is crucial. , In addition, oral lesions can be present in 30%–40% of cases and are as polymorphic as their cutaneous counterparts. Oral findings may be the sole clinical finding in as many as 61% of cases. Because oral lesions are highly contagious, stomatologists/dentists undergo academic training that makes their participation in multi-professional teams important for diagnosis and treatment of STDs, especially syphilis and HIV infection. A recent paper in The Lancet Infectious Diseases entitled “The rise of syphilis: a call to action for dermatologists” called attention to the alarming surge in cases of syphilis and the crucial role dermatologists can play in addressing this public health concern. In practice, both dermatologists and stomatologists can play roles in public health systems by guiding patients with syphilis, mainly by performing early and accurate diagnosis and referring patients to adequate treatment. Scientometrics is a useful tool that utilizes bibliometric and citation data to assess scientific output and research trend of a specific research field. Most bibliometric/scientometric analyses of STDs focus on many aspects of HIV, , , with no relevant study on syphilis. Therefore, the objective of the current study was to investigate and compare the scientometric characteristics and trends of syphilis publications by dermatologists and stomatologists. Understanding the scientometrics of syphilis will serve as a call to action for both dermatologists and stomatologists and contribute to intervention healthcare programs to control syphilis. 

A literature search utilized the Scopus database, as done in previous bibliometric analyses. , , , Scopus provides the most comprehensive overview of the global research output and has a low likelihood of article omissions compared to other databases. , , Medical subject term “syphil∗” in the Title was used in the literature search to retrieve all the papers on syphilis, without restriction to paper type and year of publication. The asterisk is a wildcard used in place of any number of characters for the most comprehensive search of relevant literature. Only English language literature was included because it is an international language of knowledge exchange. In clinical practice, dermatologists and stomatologists generally belong to the dermatology and stomatology affiliation, respectively. Hence, the papers with the word (“derm∗“) and (dent∗ OR oral OR stomatolog∗) in the affiliation generally represent scientific output of dermatologists and stomatologists, respectively. Accordingly, respective syphilis-related publications by dermatologists and stomatologists were retrieved. The scientometric characteristics of all the eligible articles were reviewed. The following information was recorded as follows: publication year, title, abstract, keywords, citation count, paper type, journal, authorship, affiliation, and country/region of origin. A list of 160 index keywords, journals, authors, affiliation, and country/region were automatically recognized in the order of highest to lowest frequency by the Scopus database. Data search and extraction were performed independently by two investigators, and discrepancy of results was resolved in a consensus symposium. Microsoft Office Excel 365 was used for index model building, and the Bibliometrix Biblioshiny R-package software was used for bibliometric statistics. In this descriptive study, variables are presented as numbers and percentages. No comparisons were made, and thus no P -values were set. All raw data utilized in this study were sourced from publicly available database. Human participants or animals were not involved in this investigation. Therefore, ethical approval was not applicable. 

Bibliometric characteristics With the search strategy algorithm, 18,120 papers on syphilis were published until the time of the search. A total of 1,981 (10.9%) and 201 (1.1%) papers were published by dermatologists and stomatologists, respectively. A illustrates the number and distribution of their paper types. To assess scientific influence of the academics, the citations of their papers were retrieved ( B). The total citation count was 18,629 and the h index was 52 for syphilis publications by dermatologists. The respective values for stomatologists were 2,376 and 25. The detailed information on publication year, title, journal, citation count, authors, affiliation, keywords, and document types of the top-100 most-cited papers on syphilis are presented in . Among the top-100 papers, 12 papers were contributed by dermatologists ( ) and one by stomatologists ( ). To further clarify the treads of scientific output concerning syphilis, we assessed the annual number and accumulated citation count of the papers during 2008–2023. The annual number of the publications by dermatologists spirally raised from 24 to 88 during 2008–2023 ( C). The accumulated citations of the papers stably increased from 333 to 1534 during this period ( D). The annual number of the publications by stomatologists slightly increased from 4 to 14 during 2008–2023, and the accumulated citations of the papers slightly increased from 50 to 211 during this period. displays cloud graphs of journal of publications, contributing authors, institutions, and countries/regions. presents the journal of publication, contributing authors, institutions, and countries/regions of origin with largest number of articles (rank, 1–10). Research characteristics Based on the frequency of keywords in all included papers, we highlighted the analysis of research characteristics of the papers on syphilis by dermatologists and stomatologists. The common keywords, study design, drug use, and syphilis-related disorders by dermatologists and stomatologists were identified. Common keywords, such as male, T pallidum , benzathine penicillin, human immunodeficiency virus (HIV) infection, differential diagnosis, and syphilis serology were similar in the publications by both dermatologists and stomatologists ( A). Most study designs ( B) and drug use ( C) were similar in the publications by both dermatologists and stomatologists, with slightly different order. Among these drugs, ceftriaxone and tetracycline were more used by dermatologists, while probenecid and prednisolone were mentioned in the publications by stomatologists. As expected, related disorders, such as secondary syphilis, HIV infection, cutaneous syphilis, neurosyphilis, congenital syphilis, lymphadenopathy, chancre, gonorrhea, erythema, rash, and papule, were common concerns in the publications by both dermatologists and stomatologists. To elucidate the respective research directions and concerned topics, we further analyzed the distinctive keywords of the papers on syphilis by dermatologists and stomatologists ( A). Concerning diagnostics, skin biopsy, skin, reagin test, sensitivity/specificity, antibody titer, bacterium antibody, blood, cerebrospinal fluid, computer assisted tomography, and reaginic antibody were distinctive keywords for dermatologists. Oral biopsy, tongue, palate, lip, oral manifestations, diagnostic error, and nuclear magnetic resonance imaging were distinctive keywords for stomatologists. Distinctive keywords of infant, pregnancy complications, lymphocytic infiltration, spirochete, and genetics were mainly used by dermatologists. Distinctive keywords used by stomatologists were questionnaire, awareness, infection risk, attitude to health, sexual health, oral sex, and unprotected sex. Interestingly, related disorders, such as latent syphilis, psoriasis, genital ulcer, fever, alopecia, headache, maculopapular rash, and pruritus, were mainly mentioned by dermatologists. Related disorders mentioned by stomatologists were mouth ulcer, mouth lesion, granuloma, hepatitis B, hepatitis C, thrush, and tuberculosis ( B). 

With the search strategy algorithm, 18,120 papers on syphilis were published until the time of the search. A total of 1,981 (10.9%) and 201 (1.1%) papers were published by dermatologists and stomatologists, respectively. A illustrates the number and distribution of their paper types. To assess scientific influence of the academics, the citations of their papers were retrieved ( B). The total citation count was 18,629 and the h index was 52 for syphilis publications by dermatologists. The respective values for stomatologists were 2,376 and 25. The detailed information on publication year, title, journal, citation count, authors, affiliation, keywords, and document types of the top-100 most-cited papers on syphilis are presented in . Among the top-100 papers, 12 papers were contributed by dermatologists ( ) and one by stomatologists ( ). To further clarify the treads of scientific output concerning syphilis, we assessed the annual number and accumulated citation count of the papers during 2008–2023. The annual number of the publications by dermatologists spirally raised from 24 to 88 during 2008–2023 ( C). The accumulated citations of the papers stably increased from 333 to 1534 during this period ( D). The annual number of the publications by stomatologists slightly increased from 4 to 14 during 2008–2023, and the accumulated citations of the papers slightly increased from 50 to 211 during this period. displays cloud graphs of journal of publications, contributing authors, institutions, and countries/regions. presents the journal of publication, contributing authors, institutions, and countries/regions of origin with largest number of articles (rank, 1–10). 

Based on the frequency of keywords in all included papers, we highlighted the analysis of research characteristics of the papers on syphilis by dermatologists and stomatologists. The common keywords, study design, drug use, and syphilis-related disorders by dermatologists and stomatologists were identified. Common keywords, such as male, T pallidum , benzathine penicillin, human immunodeficiency virus (HIV) infection, differential diagnosis, and syphilis serology were similar in the publications by both dermatologists and stomatologists ( A). Most study designs ( B) and drug use ( C) were similar in the publications by both dermatologists and stomatologists, with slightly different order. Among these drugs, ceftriaxone and tetracycline were more used by dermatologists, while probenecid and prednisolone were mentioned in the publications by stomatologists. As expected, related disorders, such as secondary syphilis, HIV infection, cutaneous syphilis, neurosyphilis, congenital syphilis, lymphadenopathy, chancre, gonorrhea, erythema, rash, and papule, were common concerns in the publications by both dermatologists and stomatologists. To elucidate the respective research directions and concerned topics, we further analyzed the distinctive keywords of the papers on syphilis by dermatologists and stomatologists ( A). Concerning diagnostics, skin biopsy, skin, reagin test, sensitivity/specificity, antibody titer, bacterium antibody, blood, cerebrospinal fluid, computer assisted tomography, and reaginic antibody were distinctive keywords for dermatologists. Oral biopsy, tongue, palate, lip, oral manifestations, diagnostic error, and nuclear magnetic resonance imaging were distinctive keywords for stomatologists. Distinctive keywords of infant, pregnancy complications, lymphocytic infiltration, spirochete, and genetics were mainly used by dermatologists. Distinctive keywords used by stomatologists were questionnaire, awareness, infection risk, attitude to health, sexual health, oral sex, and unprotected sex. Interestingly, related disorders, such as latent syphilis, psoriasis, genital ulcer, fever, alopecia, headache, maculopapular rash, and pruritus, were mainly mentioned by dermatologists. Related disorders mentioned by stomatologists were mouth ulcer, mouth lesion, granuloma, hepatitis B, hepatitis C, thrush, and tuberculosis ( B). 

Despite advancements in education and control, the public's understanding of STDs remains fraught with challenges. The resurgence of syphilis cases worldwide highlights the continued relevance of STDs in public health discourse, underpinning the vital role of dermatologists in diagnosis, treatment, and broader preventive measures. However, the results of this bibliometric study revealed that dermatologists contributed 10.9% of all the papers on syphilis, and participated in 12 of 100 most-cited papers on syphilis. To some extent, this might be a reason that a paper newly published in The Lancet Infectious Diseases launched a call to action for dermatologists in the rise of syphilis. Where syphilis once was a skin disease studied intently and diagnosed clinically by dermatologists, other clinicians began to assume the responsibility when methods of laboratory diagnosis evolved and awareness grew that syphilis is “less and less a skin disease”. These highlighted an opportunity for dermatologists to become reengaged, particularly with the resurgence of syphilis cases. Bibliometric characteristics including journals of publications, authors, institutions, and research keywords were identified in sequence. These would aid clinicians and researchers in choosing target journals, finding potential collaborators or partner institutions, as well as promoting mutual understanding and more reciprocal cooperation regarding syphilis research. The rise in the incidence of syphilis necessitates a coordinated effort. Although syphilis is well-known to dermatologists, familiarity of its manifestations is essential among primary care practitioners and other concerned specialists, such as gynecologists, pediatricians, urologists, and stomatologists. Collaboration, education, and proactive serological testing are important components of a comprehensive response to this public health threat. The importance of the consulting and working multidisciplinary among different specialists must be highlighted. By championing such initiatives, the impact of this resurgent epidemic can be mitigated. To comprehend the research directions and concerned topics of syphilis, the research keywords of the publications by dermatologists and stomatologists were analyzed. The complexity and diversity of clinical manifestations of syphilis and its related disorders, such as HIV infection, neurosyphilis, congenital syphilis, latent syphilis, lymphadenopathy, chancre, gonorrhea, erythema, rash, papule, psoriasis, genital ulcer, fever, alopecia, headache, and pruritus, often referred to as the great mimic, underscore the importance of dermatologists. HIV and syphilis have a complex bilateral relationship. Besides sharing risk factors, the presence of a mucosal lesion favors the penetration of a virus. A chancre is a synonym of primary syphilis or reinfection. Patients with a history of syphilis, even if appropriately treated, are significantly less likely to develop a chancre. Interestingly, dermatologist's keywords did not contain terms related to the mouth, while stomatologist's keywords included terms related to skin/cutaneous. This might suggest that the manifestations in the mouth appear earlier than those on the skin, or the dermatologists may neglect the mouth signs. Oral mucosal manifestations can be present in 30–40% of syphilis patients and are as polymorphic as their cutaneous counterparts. Some papers reported that first signs of this disease appeared in oral mucosa, preceding other presentations. The tongue was most common affected (32−43%), followed by the lips (25−40%) and palate (20−34%). Oral lesions of syphilis can be seen in all three stages, most commonly in the second stage. Oral chancre observed in primary syphilis is often characterized as a painless ulcer, measuring 1−2 cm, with a firm and rolled border. Patients often progress to the secondary stage 2–12 weeks after the chancre appears. Secondary syphilis presents multiple and generally symptomatic classic chancre-ulcers and mucous patches, which constitute 80% of presentations of secondary syphilis. Tertiary syphilis presents after many years in the setting of untreated syphilis and is separated into gummatous, neuro, and cardiovascular syphilis. Because oral lesions are highly contagious, the reliability of correct diagnosis aids adequate management, reduces the infection chain, and reduces the risk of transmission to health professionals. Laboratory diagnosis confirmation of syphilis is performed using serological tests. The asymptomatic nature of the latent stage means diagnosis is only possible with serological screening tests. For general patients, the diagnosis needs an index of clinical suspicion during anamnesis. Dentists and clinicians should include anamnesis regarding the sexual behaviors of their patients, and be prepared to recognize and diagnose oral and systemic manifestations of STDs, especially syphilis. In medicine and dentistry, anamnesis about sexual behavior is an essential step to the proper diagnosis and treatment of disease. Anamnesis should be performed routinely, particularly when symptoms suggest sexually transmitted infections, individuals at high risk of syphilis, including males, MSM, people with HIV infection, history of incarceration, sex work, military service, and drug use, and also considering factors that include local prevalence, socioeconomic determinants, and sexual network characteristics. In summary, this study is the first comprehensive report of the scientometric characteristics of syphilis publications by dermatologists and stomatologists. In the modern context, both dermatologists and stomatologists play roles in providing early recognizing and timely diagnosis of syphilis, advocating for public health campaigns aimed at increasing awareness, and improving access to care for at-risk patient populations. 

The authors have no conflicts of interest relevant to this article. 

