The evolution of primary hyperparathyroidism publications and global productivity from past to present: A bibliometric analysis during 1980 to 2022

Abstract

The aim of this study was to perform a descriptive analysis of scientific articles about primary hyperparathyroidism (PHPT) using bibliometric approaches. By analyzing the links between the various research components (authors, journals, institutions, countries) of the academic outputs, it was aimed to summarize the intellectual structure of PHPT, identify recent research trends, and determine the global productivity. Three thousand nine hundred fifty-four articles on PHPT published between 1980 and 2022 were pulled from the Web of Science database and analyzed using bibliometric approaches. Bibliometric network visualization maps were used to identify trending topics, citation analysis, and international collaborations. Spearman correlation coefficient was used for correlation analysis. The 3 most prolific authors are Bilezikian JP. (n = 87), Silverberg SJ. (n = 72) and Akerstrom G. (n = 57). The top 3 most productive institutions were Columbia University (n = 133), Udice French Research Universities (n = 127) and Uppsala University (n = 98). The top 3 most productive journals were Surgery (n = 216), Journal of Clinical Endocrinology and Metabolism (n = 201) and World Journal of Surgery (n = 148). The top 3 contributing countries to the PHPT literature were United States of America (n = 1062, 26.8%), Italy (346, 8.7%) and United Kingdom (274, 6.9%). The most studied topics from past to present are parathyroidectomy, hypercalcemia, parathyroid hormone/adenoma/glands, calcium/calcimimetics, scintigraphy/sestamibi, bone mineral density, ultrasound, vitamin D, osteoporosis, minimally invasive parathyroidectomy, brown tumor, nephrocalcinosis/nephrolithiasis, multiple endocrine neoplasia type 1, normocalcemia, pregnancy, imaging/preoperative imaging, parathyroid cancer/carcinoma, asymptomatic primary hyperparathyroidism, and cinacalcet. The trending topics in recent years were normocalcemic primary hyperparathyroidism, trabecular bone score, children, CDC73, microwave ablation, radiofrequency ablation, denosumab, cinacalcet, preoperative imaging, imaging, diagnosis, CT, PET, PET/CT, 4D/CT, SPECT/CT, F-18-fluorocholine, quality of life, fractures, and metabolic syndrome. We can say that there will be an increasing research trend on PHPT in the coming years. In addition to the Western countries such as the United States and European countries with large economies, Japan and Turkey were also identified as leading countries in the development of the PHPT literature. This study provides significant information about the intellectual structure and global productivity of PHPT to clinicians and other researchers interested on PHPT.

1. Introduction

Primary hyperparathyroidism (PHPT) is a disorder characterized by the excessive secretion of parathyroid hormone (PTH) from 1 or more of the parathyroid glands, resulting in hypercalcemia and disrupted calcium homeostasis. It is typically caused by a benign tumor or hyperplasia of the parathyroid glands, leading to increased PTH production and subsequent elevation of serum calcium levels.^[1–3]

PHPT may also be associated with inherited endocrine disorders, primarily multiple endocrine neoplasia type 1, MEN2A, and MEN4, hereditary hyperparathyroidism-jaw tumor syndrome, familial isolated hyperparathyroidism, familial hypocalciuric hypercalcemia, and neonatal severe hyperparathyroidism.^[3,4] Advances in genetics have led to the estimation that more than 10% of patients with PHPT have a mutation in 1 of 11 genes related with syndromic and non-syndromic forms of PHPT.^[5]

The diagnosis of PHPT is biochemical. There are evident signs and symptoms in symptomatic PHPT patients, whereas there are no disease-specific symptoms in asymptomatic PHPT patients.^[2,3,6] The introduction of multi-channel screening tests at the start of the 1970s signaled a significant change in the incidence and clinical profile of PHPT.^[2,7] Previously (1965–1974), the mean yearly incidence had been reported to be 7.8 ± 1.2 cases per 100,000, and following the start of routine serum calcium measurement, this increased to 51.1 ± 9.6 cases per 100,000.^[8] The most recent increase in the incidence is basically due to routine serum calcium determination or calcium and PTH measurements in studies of osteoporosis.^[4]

In a study conducted in the United States of America, the prevalence of PHPT in the general population was estimated to be 0.86%.^[9] The prevalence of normocalcemic and hypercalcemic PHPT in Canada was evaluated by the Canada Multicentre Osteoporosis Study, and was reported to be 3.3% and 1.4%, respectively.^[10] PHPT has the highest incidence in postmenopausal females, and is the third most common endocrine disorder.^[1] The incidence of PHPT is similar in premenopausal females and males, but for unknown reasons it is 3 to 5-fold higher after menopause.^[4,11] This rate varies from close to 1 in individuals aged < 40 years, to 5-fold greater in those older than 75 years, and the highest incidence is seen in females aged 50 to 60 years.^[1] However, there is a need for prospective studies to be conducted simultaneously in different parts of the world for better definition of the prevalence and incidence of the hypercalcemic and normocalcemic forms of PHPT.^[4]

Together with the advances in the efficacy and reliability of surgical techniques, the most recent guidelines for PHPT treatment recommend that minimally invasive parathyroidectomy is indicated for symptomatic patients. Asymptomatic patients who are not compatible with the surgical guidelines can be followed up without surgery for at least 1 year, but observation and pharmacological treatment are less effective and less cost-effective than surgery even when the patient is accepted as asymptomatic.^[2] The medical treatment of mild disease can be administered with biphosphonates, hormone replacement therapy, and calcimimetics.^[1] It is recommended that all patients who will be managed without surgery have a diet rich in vitamin D, and the supplementation of vitamin D with a target level of > 30 ng/mL is recommended in PHPT.^[1,5,12] Parathyroidectomy in patients with PHPT results in the normalization of biochemical values and increased bone mineral density.^[13] Familial PHPT, re-operative parathyroidectomy and parathyroid carcinoma are difficult conditions which require special interest and specialization.^[2]

Bibliometry is a new type of quantitative research, which has become more widespread in recent years to be able to evaluate the literature related to a specific subject.^[14–20] With the statistical analysis of literature related to a certain subject, the current research status of the subject can be understood and important findings of countries, research institutions, researchers, important journals, and collaborations of research teams can be presented for future research.^[16–19]

There has been no bibliometric study on PHPT in the literature to date. The aim of this study was to perform a descriptive analysis of scientific articles about PHPT using bibliometric approaches. The main research questions we aimed to address in our study are as follows: to quantitatively demonstrate the scientific productivity of authors, institutions, journals, and countries in the field of PHPT using basic statistical analyses, to predict future publication numbers using exponential smoothing forecast, to determine the knowledge structure of the PHPT field through co-word analysis, and to identify emerging trend topics that have received increased focus in recent years. Additionally, we aimed to identify influential studies through citation analysis and to determine the field’s structure through co-citation analysis.

2. Material and methods

2.1. Research strategy

The web of science (WoS), (by Clarivate Analytics) was used to access the bibliometric outputs of articles published on PHPT. The period included in the analyses of the articles was defined as 1980 to 2022. Using the keyword of “Primary hyperparathyroidism” in the search strategy, all the publications with this in the title were accessed. Abbreviations and different spellings were taken into consideration in the search strategy. If researchers wish to access similar documents, the following codes can be used: [“primary hyperparathyroid* (primary hyperparathyroidism, primary hyperparathyroid etc.)] OR [“Primary hyper-parathyroid*” (primary hyperparathyroidism, primary hyper/parathyroidism, primary hyperparathyroidism etc.)] OR [(Title = “PHPT” AND Topic = “primary hyperparathyroid*”)]. For this study, the date of access was April 1, 2023, but search results from WoS may vary according to different access dates as articles published online may be indexed in later months.

2.2. Statistical analysis

VOSviewer software (Version 1.6.18, Leiden University) was used to perform the bibliometric analyses (trend topic, international relationships, and citation analyses).^[21] VOSviewer is a software package used for visualizing bibliometric analyses and creating network maps. It provides text mining capabilities to construct and visualize co-occurrence networks of keywords found in articles. The analysis of keyword co-occurrence is a bibliometric method used to map the research field. Co-occurrence analysis examines the presence of keyword pairs in different publications to determine relationships between the words used in the texts. There is a relationship between co-word analysis and co-citation analysis. While co-word analysis focuses on keywords in documents, co-citation analysis focuses on citations. Co-citation analysis allows for the mapping of the structure of a research field through the shared citation patterns among document pairs.^[17–21]

Statistical analyses were performed using SPSS vn. 22.0 software (SPSS Inc., Chicago, IL). Using priori publication trends, the Exponential Smoothing prediction taking seasonal adjustment into consideration was used in the Microsoft Office Excel to predict the future publication trend. A global productivity map on the subject of PHPT was drawn using an open access website (https://app.datawrapper.de). Before the correlation analyses, conformity of the data to normal distribution was examined with the Kolmogorov-Smirnov test, Q-Q plot, and histogram. The Spearman correlation coefficient was used in the correlation analyses between the data obtained from the World Bank^[22] and from the WoS. The level of statistical significance was defined as P < .05.

3. Results

A total of 6509 publications were detected which were published on the subject of PHPT between 1980 and 2022 in the literature. Of these, 68 studies published in Veterinary Sciences were excluded. The distribution of the remaining 6441 publications was as follows: Article (3954, 61.4%), Meeting Abstract (1257, 19.5%), Review Article (350, 5.4%), Letter 346, 5.3%), Proceeding Paper (318, 4.9%) and other types of publications (Editorial Materials, Book Chapters, and Discussions etc.). Bibliometric analyses were performed on 3954 articles, of which 3564 (90.1%) were in English and the others were in the following languages: French (127), German (121), Spanish (90), Russian (18), Portuguese (9), Italian (7), Turkish (6), Japanese (3), Korean (3), Polish (3), Czech (2), and Icelandic (1).

Of the articles evaluated, 91.4% (n = 3612) were indexed in the Science Citation Index Expanded, and 7.5% (n = 296) in the Emerging Sources Citation Index. The other few articles were indexed in the Social Sciences Citation Index.

3.1. The leading research areas on the subject of primary hyperparathyroidism

The top 15 research areas with the most articles published on PHPT were determined to be Endocrinology Metabolism (n = 1247), Surgery (1167), Medicine General Internal (640), Radiology Nuclear Medicine Medical Imaging (222), Medicine Research Experimental (170), Otorhinolaryngology (122), Oncology (99), Pediatrics (81), Urology Nephrology (80), Obstetrics Gynecology (54), Pathology (45), Rheumatology (37), Medical Laboratory Technology (34), Pharmacology Pharmacy (32) and Peripheral Vascular Disease (31).

3.2. Past and future publication trends of articles on primary hyperparathyroidism

The graph showing the distribution of the number of articles by year in the past and predicted for the future (considering seasonal adjustment) is shown in Figure 1. According to the Exponential Smoothing prediction results, it was predicted that 177 articles on PHPT would be published in 2023 (Confidence Interval%: 146–208) and 219 in 2027 (Confidence Interval%: 176–261) (Fig. 1).

Figure 1.

A line graph illustrating the changes in published articles on primary hyperparathyroidism over the years, with a forecast for the next five years.

3.3. The leading authors on the subject of primary hyperparathyroidism

The top 10 authors contributing the most to the literature on PHPT were determined to be Bilezikian JP. (Number of articles = 87), Silverberg SJ. (n = 72), Akerstrom G. (n = 57), Ljunghall S. (n = 53), Rastad J. (n = 52), Marcocci C. (n = 50), Minisola S. (n = 47), Bergenfelz A. (n = 45), Mosekilde L. (n = 41), and Chen H. (n = 39). For the coauthor citations analysis, a threshold of 15 (minimum number of documents of an author) was selected using the VOSviewer package. The citation network visualization was presented in Figure 2, comprising 44 authors who have produced at least 15 articles. The citation network among the authors exhibited 4 distinct clusters. When determining the sizes of the circles in the network map, normalized citation values were used for weighting. The normalized citation count of an author is obtained by dividing their citation count by the average citation count received by all authors within the same year. Normalization corrects for the fact that authors with older works have more time to receive citations compared to authors with more recent works.

Figure 2.

The author citation network visualization map. Different clusters are represented by different colors. The size of the circle indicates the magnitude of the total citation count. The connection and proximity between two articles describe the citation relationship between them, and the thickness of the lines represents the strength of citation links.

3.4. The leading institutions on the subject of primary hyperparathyroidism

The top 20 institutions in respect of the contributions to literature on the subject of PHPT were found to be Columbia University (Number of articles = 133), Udice French Research Universities (127), Uppsala University (98), University of California System (96), Assistance Publique Hopitaux Paris (91), Uppsala University Hospital (88), Mayo Clinic (72), Sapienza University Rome (68), Aarhus University (67), Universite Paris Cite (67), Lund University (66), Karolinska Institutet (65), University of Pisa (65), U.S. Department of Veterans Affairs/Veterans Health Administration (65), University of California San Francisco (58), Institut National De La Sante Et De La Recherche Medicale Inserm (55), Karolinska University Hospital (53), Harvard University (52), University of Copenhagen (51), Skane University Hospital (49), University of Texas System (48), Yale University (47), Aix Marseille Universite (44), and Assistance Publique Hopitaux De Marseille (43).

A clustering network map obtained through co-authorship analysis was presented in Figure 3A, based on a collaborative analysis involving 45 institutions among the 3191 institutions publishing at least 15 articles (threshold = 15) on the subject of PHPT.

Figure 3.

(A) Co-authorship network map between institutions. (B) The journal citation network visualization map. (C). Co-authorship network map between countries. Different clusters are represented by different colors. The connection and proximity between two authors, journals, or countries describe the collaboration relationship.

3.5. The leading journals on the subject of primary hyperparathyroidism

The 3954 articles published on PHPT were published in 811 different scientific journals. The top 47 journals (≥15 articles published) contributing to the literature on PHPT, the total number of citations received by the journals, and the average number of citations per article received by the journals are shown in Table 1.

Table 1.

The 47 most productive scientific journals that have published 15 or more articles on primary hyperparathyroidism.

Journals	NA	NC	AC	Journals	NA	NC	AC
Surgery	216	7713	35.7	Internal Medicine	23	182	7.9
Journal of Clinical Endocrinology & Metabolism	201	14,533	72.3	Annales D Endocrinologie	22	109	5.0
World Journal of Surgery	148	4857	32.8	Experimental and Clinical Endocrinology & Diabetes	22	242	11.0
Clinical Endocrinology	107	3354	31.3	Acta Endocrinologica-Bucharest	21	51	2.4
European Journal of Endocrinology	74	2168	29.3	Chirurg	21	137	6.5
Journal of Endocrinological Investigation	66	1035	15.7	Acta Endocrinologica	20	342	17.1
Endocrine Practice	56	587	10.5	Journal of Surgical Research	19	208	10.9
American Journal of Surgery	53	1087	20.5	International Journal of Endocrinology	19	225	11.8
Langenbecks Archives of Surgery	51	888	17.4	Endocrinology Diabetes and Metabolism Case Reports	18	51	2.8
Journal of Bone and Mineral Research	48	3100	64.6	Journal of Internal Medicine	18	627	34.8
American Surgeon	43	726	16.9	Laryngoscope	18	233	12.9
Annals of Surgical Oncology	39	1120	28.7	Mineral and Electrolyte Metabolism	18	349	19.4
Annals of Surgery	35	3108	88.8	Annals of the Royal College of Surgeons of England	17	180	10.6
British Journal of Surgery	34	1282	37.7	Endocrine Connections	17	137	8.1
Endocrine	34	404	11.9	Osteoporosis International	17	364	21.4
Bone	33	1269	38.5	Revista Medica De Chile	16	46	2.9
Endocrine Journal	33	422	12.8	American Journal of Medicine	15	885	59.0
Archives of Surgery	32	2079	65.0	Annales Chirurgiae Et Gynaecologiae	15	174	11.6
Journal of Bone and Mineral Metabolism	28	298	10.6	Annales De Chirurgie	15	87	5.8
Calcified Tissue International	27	409	15.1	Endocrinology and Metabolism Clinics of North America	15	395	26.3
Postgraduate Medical Journal	26	312	12.0	Endocrinologist	15	29	1.9
Hormone and Metabolic Research	25	231	9.2	Journal of Nuclear Medicine	15	564	37.6
Journal of the American College of Surgeons	24	913	38.0	Surgery Today	15	115	7.7
Clinical Nuclear Medicine	23	449	19.5

AC = average citation per document, NA = Number of articles, NC = Number of citations.

The clustering network map obtained through co-authorship analysis involving 45 journals that have published at least 15 articles (threshold = 15) on the subject of PHPT was presented in Figure 3B.

3.6. The countries active on the subject of primary hyperparathyroidism

A clustering network map obtained through co-authorship analysis was presented in Figure 3C, based on a collaborative analysis involving 46 countries among the 95 countries publishing at least 10 articles (threshold = 15) on the subject of PHPT.

The world map of the number of articles published on PHPT by countries, shown according to color density and the graph showing the top 20 countries contributing the most to literature are shown in Figure 4. The top 20 countries making the most academic contribution to the literature on PHPT were determined to be the United States of America (1062, 26.8%), Italy (346, 8.7%), the United Kingdom (274, 6.9%), France (245, 6.2%), Sweden (243, 6.1%), Japan (199, 5%), Turkey (191, 4.8%), Germany (185, 4.6%), Denmark (132, 3.3%), Spain (129, 3.2%), China (123, 3.1%), India (119, 3%), Canada (103, 2.6%), Australia (76, 1.9%), Austria (75, 1.8%), Switzerland (67, 1.6%), the Netherlands (66, 1.6%), Brazil (61, 1.5%), Belgium (45, 1.1%), Israel (45, 1.1%), and Poland (39, 1%).

Figure 4.

A bar graph displaying the top 20 nations with the most primary hyperparathyroidism articles published, as well as a globe productivity map displaying the countries’ contribution to the literature.

International collaboration analysis was applied to 79 countries with articles published on PHPT and scores were calculated showing the strength of collaboration. According to these scores, the 10 countries with the highest levels of collaboration were determined to be the United States of America (Score = 260), Italy (159), England (95), Germany (85), Denmark (83), France (80), the Netherlands (80), Switzerland (76), Canada (75) and Brazil (67).

A statistically significant correlation at a high level was determined between the number of articles of the countries and the gross domestic product (GDP), which is a marker of the economic size of a country, and Gross Domestic Product per capita (GDP per capita) values (R = 0.742, P < .001; R = 0.721, P < .001, respectively).

3.7. Citation analysis of the articles on the subject of primary hyperparathyroidism

The titles, authors, journals where published, year of publication, total number of citations received by the articles, and the average number of citations per year of the top 20 articles that received the most citations (> 240) from the total 3954 articles are shown in Table 2. The citation network map, derived from these 20 studies among a total of 3954 articles that meet the threshold value of at least 240 citations, was presented in Figure 5A.

Table 2.

The top 20 most cited articles (more than 240 citations) on primary hyperparathyroidism.

No	Article	Author	Journal	PY	TC	AC
1	Primary hyperparathyroidism - incidence, morbidity, and potential economic-impact in a community	Heath H. et al	New England Journal of Medicine	1980	887	20.16
2	Guidelines for the management of asymptomatic primary hyperparathyroidism: summary statement from the fourth international workshop	Bilezikian JP. et al	Journal of Clinical Endocrinology & Metabolism	2014	735	73.5
3	A 10-yr prospective study of primary hyperparathyroidism with or without parathyroid surgery	Silverberg SJ. et al	New England Journal of Medicine	1999	624	24.96
4	The American Association of Endocrine Surgeons guidelines for definitive management of primary hyperparathyroidism	Wilhelm SM. et al	JAMA Surgery	2016	534	66.75
5	A systematic review of the diagnosis and treatment of primary hyperparathyroidism from 1995–2003	Ruda JM. et al	Otolaryngology-Head and Neck Surgery	2005	482	25.37
6	Skeletal disease in primary hyperparathyroidism	Silverberg SJ. et al	Journal of Bone and Mineral Research	1989	473	13.51
7	Six hundred fifty-six consecutive explorations for primary hyperparathyroidism	Udelsman R.	Annals of Surgery	2002	437	19.86
8	Reduced immunostaining for the extracellular Ca sensing receptor in primary and uremic secondary hyperparathyroidism	Kifor O. et al	Journal of Clinical Endocrinology & Metabolism	1996	415	14.82
9	Incidence and prevalence of primary hyperparathyroidism in a racially mixed population	Yeh MW. et al	Journal of Clinical Endocrinology & Metabolism	2013	365	33.18
10	The natural history of primary hyperparathyroidism with or without parathyroid surgery after 15 yr	Rubin MR. et al	Journal of Clinical Endocrinology & Metabolism	2008	361	22.56
11	NIH Conference - diagnosis and management of asymptomatic primary hyperparathyroidism - consenus development conference statement	Potts JT.	Annals of Internal Medicine	1991	355	10.76
12	Primary hyperparathyroidism - changes in the pattern of clinical presentation	Mundy GR. et al	Lancet	1980	315	7.16
13	Cinacalcet hydrochloride maintains long-term normocalcemia in patients with primary hyperparathyroidism	Peacock M. et al	Journal of Clinical Endocrinology & Metabolism	2005	309	16.26
14	Unilateral versus bilateral neck exploration for primary hyperparathyroidism - A prospective randomized controlled	Bergenfelz A. et al	Annals of Surgery	2002	274	12.45
15	Primary hyperparathyroidism in the 1990s - choice of surgical-procedures for this disease	Kaplan EL. et al	Annals of Surgery	1992	271	8.47
16	The histomorphometry of bone in primary hyperparathyroidism - preservation of cancellous bone-structure	Parisien M. et al	Journal of Clinical Endocrinology & Metabolism	1990	266	7.82
17	Incidence of primary hyperparathyroidism in Rochester, Minnesota, 1993–2001: An update on the changing epidemiology of the disease	Wermers RA. et al	Journal of Bone and Mineral Research	2006	265	14.72
18	Surgical treatment of primary hyperparathyroidism - an institutional perspective	Vanheerden JA. and Grant CS.	World Journal of Surgery	1991	264	8
19	Primary hyperparathyroidism and the risk of fracture: A population-based study	Khosla S. et al	Journal of Bone and Mineral Research	1999	260	10.4
20	The superiority of minimally invasive parathyroidectomy based on 1650 consecutive patients with primary hyperparathyroidism	Udelsman R. et al	Annals of Surgery	2011	243	18.69

AC = average citations per year, PY = publication year, TC = total citation.

Figure 5.

(A) Network visualization map for citation analysis. (B) Network visualization map for co-citation analysis. Each circle is labeled with the first author of the article and the publication year. The color of the circle indicates the cluster to which the article is associated. The size of the circle represents the normalized citation count received by the articles, and the thickness of the lines represents the strength of co-citation links.

3.8. Co-citation analysis of the articles on the subject of primary hyperparathyroidism

In the references sections of the 3954 articles published on the subject of PHPT, a total of 33,053 publications were cited. The co-citation network map, based on 58 studies that meet the threshold value of at least 80 citations from the references, was presented in Figure 5B. In addition, the most effective studies with more than 170 co-citations were found to be those by Heath et al^[8] (1980) (Number of co-citations, NC = 375), Bilezikian et al^[5] (2014) (NC = 359), Silverberg et al^[13] (1999) (NC = 325), Bilezikian et al^[23] (2009) (NC = 281), Wilhelm et al^[2] (2016) (NC = 209), Fraser (2009) (NC = 200), Rubin et al^[7] (2008) (NC = 199), Silverberg et al^[24] (1989) (NC = 197), and Bilezikian et al^[25] (2002) (NC = 196).^[1]

3.9. Previous and current research trends on the subject of primary hyperparathyroidism

In the 3954 articles published on PHPT, a total of 2944 different key words were used. The 114 keywords that were used in 7 or more articles are shown in Table 3. The results of the cluster analysis showing the status of use of the key words together are shown in Figure 6A. According to the results of keyword analysis, the most prominent topics in articles on PHPT from the past to the present were identified as parathyroidectomy/parathyroid surgery, hypercalcemia (or hypercalcaemia)/hypercalcemic crisis/hypercalciuria, parathyroid hormone (or PTH)/parathormone/parathyroid, parathyroid adenoma, calcium/serum calcium/calcium-sensing receptor/calcimimetic(s), parathyroid scintigraphy/sestamibi (scan or scintigraphy)/technetium tc 99m sestamibi/MIBI, bone/bone density/bone mineral density, ultrasound (or ultrasonography), vitamin D/vitamin D deficiency, surgery/surgical treatment, osteoporosis, minimally invasive parathyroidectomy/surgery, brown tumor (or tumor),nephrocalcinosis/nephrolithiasis, multiple endocrine neoplasia/or type 1/multiple endocrine neoplasia type 1 , normocalcemia (or normocalcemic), parathyroid gland(s), pregnancy, parathyroid imaging/preoperative imaging/preoperative localization, parathyroid cancer/carcinoma, asymptomatic primary hyperparathyroidism and cinacalcet.

Table 3.

The 114 most frequently used keywords in published articles on primary hyperparathyroidism.

Keywords	N	Keywords	N	Keywords	N	Keywords	N
Primary hyperparathyroidism or (PHPT)	1156	Multiple endocrine neoplasia type 1	22	Focused parathyroidectomy	12	Nephrocalcinosis	8
Hyperparathyroidism	473	Vitamin D deficiency	22	Kidney stones	12	Osteocalcin	8
Parathyroidectomy	373	Fracture (s)	19	MEN1	12	Parathyroid cancer	8
Hypercalcemia (or hypercalcaemia)	306	Calcimimetic (s)	18	Prevalence	12	Parathyroid imaging	8
Parathyroid hormone (or PTH)	235	Hypocalcemia	18	Hypercalciuria	11	PET	8
Parathyroid adenoma	186	Parathyroid neoplasms	18	Localization	11	Preoperative imaging	8
Calcium	86	Technetium tc 99m sestamibi (or MIBI)	18	Normocalcemic hyperparathyroidism	11	Preoperative localization	8
Ultrasound (or ultrasonography)	79	Acute pancreatitis	17	Recurrence	11	Renal function	8
Bone mineral density	72	Bone	17	Serum calcium	11	4D-CT	7
Osteoporosis	66	Case report	17	Blood pressure	10	Carcinoma	7
Parathyroid	62	Normocalcemia (or normocalcemic)	17	Epidemiology	10	Cardiovascular disease	7
Surgery	62	Parathormone	17	F-18-fluorocholine	10	Children	7
Brown tumor (or tumor)	59	Quality of life	17	Hyperplasia	10	Chronic kidney disease	7
Sestamibi (scan or scintigraphy)	55	Scintigraphy	17	Microwave ablation	10	Complications	7
Vitamin D	51	Imaging	16	Depression	9	Denosumab	7
Nephrolithiasis	40	Parathyroid scintigraphy	16	Outcome	9	Familial hyperparathyroidism	7
Parathyroid gland (s)	40	Parathyroid surgery	16	PET/CT	9	Hypercalcemic crisis	7
Pregnancy	40	Calcium-sensing receptor	15	Radiofrequency ablation	9	Menopause	7
Adenoma	36	Hypertension	15	Spect	9	Metabolic syndrome	7
Asymptomatic primary hyperparathyroidism	34	Normocalcemic primary hyperparathyroidism	15	Thyroid	9	Mortality	7
Primary	33	Hungry bone syndrome	14	Aldosterone	8	Pheochromocytoma	7
Minimally invasive parathyroidectomy	32	Secondary hyperparathyroidism	14	Bone density	8	Polymorphism	7
Cinacalcet	31	Bilateral neck exploration	13	Breast cancer	8	Radioguided surgery	7
Minimally invasive surgery	31	Diagnosis	13	CDC73	8	Reoperation	7
Osteitis fibrosa cystica	26	Familial hypocalciuric hypercalcemia	13	Diabetes mellitus	8	Surgical treatment	7
Computed tomography (or CT)	25	Multiple endocrine neoplasia	13	Endocrine	8	Thyroid cancer	7
Parathyroid carcinoma	24	Pancreatitis	13	Hypoparathyroidism	8	Trabecular bone score	7
Parathyroid hyperplasia	23	SPECT/CT	13	Intact parathyroid hormone	8
Bisphosphonates	22	Elderly	12	Multiple gland disease	8

MEN1 = multiple endocrine neoplasia type 1, N = number of uses.

Figure 6.

(A) Network visualization map created to highlight clustering trends of primary hyperparathyroidism issues based on cluster analysis findings. Different clusters are represented by different colors. Keywords with similar colors are grouped together. The size of the circle indicates the number of keyword usages. (B) Keyword bursts network map. (C) Hotspots for Keyword bursts network map. Intensity increases from blue to red.

The keyword burst analysis network map was presented in Figure 6B, and A new map showcasing the zoomed-in view of the hotspots in this map was presented in Figure 6C. The network visualization map showing the previous and current trends of use of the key words is shown in Figure 7. The trending topics in recent years were normocalcemic primary hyperparathyroidism, trabecular bone score, children, CDC73, microwave ablation, radiofrequency ablation, denosumab, cinacalcet, preoperative imaging, imaging, diagnosis, CT, PET, PET/CT, 4D/CT, SPECT/CT, F-18-fluorocholine, quality of life, fractures, and metabolic syndrome.

Figure 7.

Based on keyword analysis, a network visualization map illustrating previous and present trends in primary hyperparathyroidism. The indicator in the lower right corner of the graphic moves from blue to red as the topicality of the subjects grows (blue-green-yellow-red). The size of the circle indicates the number of keyword usages.

The citation network visualization map of the citation analysis results showing the key words in the articles that received the most citations is shown in Figure 8. The keywords used in the most cited articles were epidemiology, prevalence, normocalcemic primary hyperparathyroidism, hypercalciuria, PET/CT, SPECT/CT, F-18-fluorocholine, bone density, children, diabetes mellitus, mortality, cardiovascular disease, menopause, blood pressure, and reoperation.

Figure 8.

A network visualization map illustrating the most frequently cited issues in primary hyperparathyroidism. The indicator in the lower right corner of the graphic moves from blue to red as the subject receives more citations (blue-green-yellow-red). The size of the circle indicates the number of keyword usages.

4. Discussion

When the distribution of the articles published on the subject of PHPT in the period 1980 to 2022 was examined, there were observed to be 3 different publication trends for the years 1980 to 2007, 2008 to 2019, and 2020 to 2022. Between 1980 and 2007, an average of 67 articles per year were published (range, 41–101). In the period 2008 to 2019, an average of 129 articles per year were published (range, 105–150). A trend started in 2020 for an increase in the number of articles with an average of 181 articles per year published in 2020 to 2022 (range 172–189). When the prediction results regarding the number of articles during the period of 2023 to 2027 are evaluated together with the past research trend, we can say that there will be an increasing research trend on PHPT in the coming years.

Of the top 20 most productive countries on the subject of PHPT, 16 are developed countries and 4 are developing countries with large economies. A statistically significant correlation at a high level was determined between the number of articles published by countries and the GDP and GDP per capita of those countries. In the bibliometric studies conducted by Kiraz et al^[17] (2021), Aykaç and Eliaçik (2022), Aliç and Hassa (2022), a significant relationship was identified between countries’ article productivity and indicators of economic development.^[18,20] Our findings are consistent with the results of these studies. However, it should be noted that besides the economic development of countries, there are several other factors that influence article productivity, such as research infrastructure (universities, research centers, well-equipped laboratories) and funding, scientific collaborations (conferences and workshops), education (training qualified human resources), and research incentives (reward systems).^[26] Our study focused only on determining the level of relationship between article productivity in the field of PHPT and GDP and GDP per capita. When evaluating the results of co-authorship analysis, it was determined that the United States and European countries (Italy, United Kingdom, Germany, Denmark, France, Netherlands, and Switzerland) were leading countries in collaboration.

In terms of quantitative contributions to the PHPT literature, the leading journals were presented in Table 1. However, when compared based on the average number of citations per published article, we can say that the journals with the highest impact are the New England Journal of Medicine (mean citations per article: 238), Nature Medicine (173), Journal of the American Society of Nephrology (172), Journal of Clinical Investigation (161), Lancet (141), Obstetrical & Gynecological Survey (135), JAMA Surgery (127), Annals of Internal Medicine (118), Nature Reviews Disease Primers (101), Cardiovascular Research (93), Annals of Surgery (89), British Medical Journal (80), International Journal of Fertility and Womens Medicine (75), American Journal of Epidemiology (73), and Journal of Clinical Endocrinology & Metabolism (72). We can say that these journals stand out for researchers who prioritize their articles to have a greater impact. Furthermore, when the collaboration network map among the journals was evaluated (Fig. 3B), it was determined that the journals formed 2 distinct main clusters (Red: focused on endocrinology, and Green: focused on surgery).

By utilizing citation and co-citation analysis, commonly employed in bibliometric research,^[14–21] we identified the influential studies on PHPT. In terms of the total number of citations, the study with the greatest impact was the study entitled “Primary hyper-parathyroidism - incidence, morbidity, and potential economic-impact in a community” by Heath et al^[8] (1980) published in the New England Journal of Medicine. The second most effective study was the Guidelines published in the Journal of Clinical Endocrinology & Metabolism.^[5] These were followed by “A 10-year prospective study of primary hyperparathyroidism with or without parathyroid surgery” by Silverberg et al^[13] (1999) published in the New England Journal of Medicine, the Guidelines published in JAMA Surgery,^[2] and a systematic review by Ruda et al^[27] (2005), published in Otolaryngology-Head and Neck Surgery. When examined in terms of the average number of citations per year, the study with the most impact (average citations per year = 73.5) was the Guidelines published by Bilezikian et al (2016).^[5] This was followed by the Guidelines published by Wilhelm et al (2018),^[2] an incidence and prevalence study by Yeh et al (2013)^[11] and studies by Ruda et al^[27] (2005) and Silverberg et al (1999).^[13] According to the number of co-citations of all the articles evaluated, the studies with the most impact were by Heath et al^[8] (1980), Bilezikian et al^[5] (2014), Silverberg et al^[13] (1999), Bilezikian et al^[23] (2009), Wilhelm et al^[2] (2016), Fraser (2009), Rubin et al^[7] (2008), Silverberg et al^[24] (1989), and Bilezikian et al^[25] (2002) idi.^[1,23] It can be recommended that researchers read these studies first.

When evaluating the citation network map among the authors (Fig. 2), it was determined that the authors formed 4 distinct clusters. The citation analysis network visualization map revealed that articles receiving the highest number of citations formed 3 different structures based on total citation count (Fig. 5A). These structures were related to guidelines and conference proceedings on PHPT management (blue cluster), the incidence and prevalence of PHPT (red cluster), and the medical and surgical treatment of PHPT (green cluster). When assessing the common citation network of PHPT (Fig. 5B), it was observed that it formed 4 different structures. These clusters were related to guidelines and conference proceedings for general PHPT definition and management (yellow cluster), the medical and surgical treatment of PHPT (blue cluster), asymptomatic and normocalcemic PHPT (green cluster), and clinical course, incidence, and prevalence (red cluster) of PHPT.

By utilizing co-word keyword analysis, a commonly used method in bibliometric research,^[14–21] we identified the trending topics in the field of PHPT. Normocalcemic PHPT is a recently defined variant, which presents with high PTH levels and normal total and ionized serum calcium levels.^[2] The trabecular bone score, which is a new gray-scale tissue analysis applied in spinal DXA imaging to estimate trabecular micro-architecture, is a new technique for the evaluation of bone-structure that improves the detection of fracture risk.^[28] Therefore, these subjects are expected to be among the recent subjects more studied. Hereditary mutations in the CDC73 gene have been detected in some families with familial isolated hyperparathyroidism, which is a condition characterized with PHPT.^[4] In recent years, there has been an increase in publications related to PHPT, which is rarely seen in children. The latest developments in preoperative imaging techniques show that this subject will continue to be an important area of research. Of the pharmacological approaches used in PHPT treatment, that denosumab and cinacalcet are among the recently studied topics shows that the benefits of pharmacological interventions will be evaluated in new studies. One of the topics studied most intensely in recent years has been the quality of life of patients with PHPT after parathyroidectomy. Although asymptomatic PHPT is defined as a condition in which the classic target organs are not affected, many patients have reported nonspecific symptoms such as fatigue, irritability, lethargy, lack of mental clarity, sleep disorders, anxiety, and depression.^[3] In a systematic review by Yadav et al^[29] (2020), in which the varying clinical profile of PHPT in the developing world was reviewed, it was reported that clinical interest had moved from symptomatic to asymptomatic disease in recent years. This suggests that it also has an effect on the increase in research into quality of life of asymptomatic patients. New quality of life questionnaires developed to evaluate the health-related quality of life of PHPT patients^[30] can be considered to have had the effect of increasing studies on this subject.

There is no bibliometric study on the subject of PHPT in the literature. Therefore, this study is of value as the first such study. However, 1 limitation of the study is that the WoS database was utilized in the literature search rather than the PubMed and Scopus databases. The reason for this was that citation and co-citation analyses cannot be performed in PubMed, and some journals with a low impact are indexed in Scopus. Compared to other databases, the WoS includes articles published in higher impact journals (almost all SCI-E).^[14,31] The preference for the use of WoS in this study was also influenced by the widespread use of WoS in other bibliometric studies in literature.^[14–20,31] A second limitation of our study is the exclusion of articles published in 2023 from the analyses. However, it should be noted that in other bibliometric studies conducted in the literature,^[17–20] articles published within an incomplete year are also not included in the analyses.

5. Conclusion

The results have been presented here of a statistical analysis of 3954 articles on the subject of PHPT, for which there has been seen to be an increasing trend for scientific output. We can say that there will be an increasing research trend on PHPT in the coming years. In addition to the Western countries such as the United States and European countries with large economies, Japan and Turkey were also identified as leading countries in the development of the PHPT literature. Based on keyword analysis, citation, and co-citation analyses, it can be said that the intellectual structure of PHPT from the past to the present consists of the following topics: clinical diagnosis and symptoms, biochemical investigations, imaging techniques, surgical treatment, genetic and molecular research, and follow-up and monitoring. There has been an increase in research on normocalcemic primary hyperparathyroidism, and in recent years, there has been a rise in studies related to imaging techniques for the diagnosis of PHPT, in parallel with advancements in technology and medical science. Thermal ablation techniques such as microwave ablation and radiofrequency ablation, which have been recently proposed as alternatives to PHPT surgery, and medications such as Cinacalcet and Denosumab used in treatment, have also been among the trending topics studied in recent years. This study provides significant information about the intellectual structure and global productivity of PHPT to clinicians and other researchers interested on PHPT.

Author contributions

Conceptualization: Hüseyin Göbüt, Hasan Bostanci.

Data curation: Hüseyin Göbüt.

Formal analysis: Hüseyin Göbüt, Hasan Bostanci.

Investigation: Hüseyin Göbüt, Hasan Bostanci.

Methodology: Hüseyin Göbüt, Hasan Bostanci.

Resources: Hüseyin Göbüt, Hasan Bostanci.

Software: Hüseyin Göbüt, Hasan Bostanci.

Supervision: Hüseyin Göbüt.

Validation: Hüseyin Göbüt.

Visualization: Hüseyin Göbüt, Hasan Bostanci.

Writing – original draft: Hüseyin Göbüt, Hasan Bostanci.

Writing – review & editing: Hüseyin Göbüt, Hasan Bostanci.