Epidemiology of Clinical Sporotrichosis in the Americas: History
Please note this is an old version of this entry, which may differ significantly from the current revision.

 Sporotrichosis is a fungal infection caused by species of the Sporothrix genus.

  • sporotrichosis
  • Sporothrix schenckii sensu stricto
  • the Americas

1. Introduction

Sporotrichosis is a fungal infection caused by thermo-dimorphic fungi species of the Sporothrix genus. Previously, the classification of the species of sporotrichosis was conducted through the classification of the Sporothrix schenckii complex, which included Sporothrix schenckii sensu stricto, Sporothrix brasiliensis (S. brasiliensis), Sporothrix globosa (S. globosa), Sporothrix luriei (S. lurieri), Sporothrix pallida (S. pallida), Sporothrix mexicana (S. mexicana), and Sporothrix chilensis (S. chilensis) [1,2]. However, since 2016, the taxonomical classification of Sporothrix has been changed into a clinical clade that includes Sporothrix schenckiiS. globosaS. brasiliensis, and S. luriei. On some occasions, the species of the environmental clade, such as S. pallidaS. mexicana, and S. chilensis may cause infection upon contact with an individual [1,2,3,4]. The infections occur mainly cutaneously or subcutaneously with lymphatic involvement [1,2,3,4]. This infection has been considered the most frequent subcutaneous mycosis in Latin America [2]. Such infections can be difficult to diagnose with the naked eye since they can be similar to infiltrative or ulcerative lesions from vascular and inflammatory disorders [1,3].
For this subcutaneous infection to develop, a direct trauma must occur first. For example, inoculation occurs when the skin is punctured by plants with thorns, gardeners are a classic case of this. Also, inoculation can occur through fomites that contact contaminated soil. For instance, people who wear sandals can suffer trauma from stones, firewood, or thorns with fungal spores on their surface [2,3]. With all the above, it can be inferred that this type of fungal infection is associated with regions where the main livelihood is agriculture, that is, in environments where the climate is tropical and subtropical. Another form of transmission, which has been increasing in recent times in some regions of the continent such as Brazil, Argentina, Paraguay, and Panama, has been reported to result from scratches, bites, pecks, and stings from different animals [1,2,3,4].
There are several techniques for detecting sporotrichosis, including Sabouraud dextrose agar cultures, lactophenol blue or erythromycin staining, histopathological studies, and PCR sequencing, among others [5,6,7] (Figure 1).
Figure 1. Sporothrix spp. culture and erythromycin staining 40×.
As for the clinical forms of sporotrichosis, various types have been described, such as the lymphocutaneous, fixed cutaneous, and, as mentioned earlier, the disseminated or hematogenous forms where both organs and tissues can be affected [5,6,7,8,9,10,11,12,13,14,15,16,17,18,19,20,21,22,23,24,25,26,27,28]. The latter is the rarest because the recommended antifungal regimens are usually effective; however, in patients with alterations in cellular immunity, these infections can spread [2,3,4].

2. Epidemiology of Sporotrichosis in North America

A total of 48 publications related to sporotrichosis were found in North America [5,6,7,8,9,10,11,12,13,14,15,16,17,18,19,20,21,22,23,24,25,26,27,28,29,30,31,32,33,34,35,36,37,38,39,40,41,42,43,44,45,46,47,48,49,50,51,52]. There were 1460 patients in total associated with infection caused by species of the genus Sporothrix. According to the previous classification, it was found that in Canada, only two case reports were found, one from Ontario and the other from Toronto [5,6]. In the US, 27 reports containing 1 clinical case were found (81.5% S. schenckii, 18.5% Sporothrix spp., S. schenckii complex, and S. schenckii sensu lato) [7,8,9,10,11,12,13,14,15,16,17,18,19,20,21,22,23,24,25,26,27,28,29,30,31,32,33]. Of these, seven cases came from California, three from Oklahoma, two cases from Kansas, Texas, Arizona, Minnesota, and Florida, one case from Michigan, Nebraska, Oregon, Pennsylvania, and finally, one case without a specific city or region. In Mexico, there were 19 reports registered with 1431 reported cases (84.7% Sporothrix spp., 14.47% S. schenckii, 0.55% S. globosa, 0.21% S. schenckii sensu stricto, 0.07% S. mexicana) [34,35,36,37,38,39,40,41,42,43,44,45,46,47,48,49,50,51,52]. Jalisco reported 1060 cases, Guerrero 150, Nayarit 23, Zacatecas 21, Michoacan 20, Guanajuato 14, Oaxaca 9, Puebla, and San Luis Potosí 8 each, Mexico City 6, Chihuahua, Nuevo León, Querétaro, and Veracruz 2 each, Baja California, Durango, State of Mexico, and Morelos 1 each, and 99 cases were reported with an unspecified city (Table 1). When classifying according to the current taxonomy [1,2,3,4], we can mention that in Canada, 50% of the sporotrichosis was due to S. schenckii and 50% to Sporothrix spp. [5,6]. In the US, it was reported that Sporothrix spp. (85.19%) and S. schenckii (14.81%) were responsible for this pathology [7,8,9,10,11,12,13,14,15,16,17,18,19,20,21,22,23,24,25,26,27,28,29,30,31,32,33]. Finally, in Mexico, 85.05% were due to Sporothrix spp., 14.33% S. schenckii, 0.55% S. globosa, and 0.07% S. mexicana [34,35,36,37,38,39,40,41,42,43,44,45,46,47,48,49,50,51,52].
Table 1. Epidemiology of Sporotrichosis in North America.
Region Country City Number of Reported Cases Vulnerable Population Diagnostic Method Type of Sporotrichosis Etiological Agents
(%)
References
Sex Age (Years) Taxonomy
Before 2017 After 2017
North America Canada Ontario 1 Male 44 PCR sequencing (ITS region) Disseminated S. schenckii S. schenckii [5]
Toronto 1 Male 78 Fungal culture,
Biopsy (Histopathology)
Lymphocutaneous S. schenckii complex Sporothrix spp. [6]
USA California 1 Female 7 Fungal culture
Biopsy (Histopathology)
Lymphocutaneous S. schenckii Sporothrix spp. [7]
Minnesota 1 Male 61 Fungal culture Disseminated S. schenckii Sporothrix spp. [8]
ND 1 Female 87 Fungal culture Lymphocutaneous on the eyelid S. schenckii Sporothrix spp. [9]
Pennsylvania 1 Male 67 Fungal culture
Biopsy (Histopathology)
Lymphocutaneous S. schenckii Sporothrix spp. [10]
Texas 1 Male 34 Fungal culture
Biopsy (Histopathology)
Disseminated Sporothrix spp. Sporothrix spp. [11]
Texas 1 Male 9 Fungal culture
Biopsy (Histopathology)
Lymphocutaneous on the eyelid S. schenckii Sporothrix spp. [12]
California 1 Female 41 Fungal culture Lymphocutaneous S. schenckii Sporothrix spp. [13]
Oregon 1 Male 53 Fungal culture Disseminated Sporothrix spp. Sporothrix spp. [14]
Oklahoma 1 Male 66 Latex agglutination test Disseminated S. schenckii Sporothrix spp. [15]
Florida 1 Male 33 month-Old Fungal culture
Biopsy (Histopathology)
Atypical lymphadenitis S. schenckii Sporothrix spp. [16]
Minnesota 1 Male 49 Fungal culture Pulmonary sporotrichosis Sporothrix spp. Sporothrix spp. [17]
Arizona 1 Male 56 Fungal culture Lymphocutaneous and disseminated (10 months later) S. schenckii Sporothrix spp. [18]
California 1 Male 39 Fungal culture Sporothrical arthritis S. schenckii Sporothrix spp. [19]
California 1 Male 89 Fungal culture
Biopsy (Histopathology)
Disseminated S. schenckii Sporothrix spp. [20]
Michigan 1 Female 57 Fungal culture
Biopsy (Histopathology)
Lymphocutaneous S. schenckii Sporothrix spp. [21]
California 1 Male 34 Latex agglutination test Chronic meningitis S. schenckii Sporothrix spp. [22]
Kansas 1 Male 33 Fungal culture
MALDI-TOF
Sporothrical arthritis S. schenckii Sporothrix schenckii [23]
Oklahoma 1 Male 44 Fungal culture
Biopsy (Histopathology)
Pulmonary sporotrichosis S. schenckii sensu lato Sporothrix spp. [24]
California 1 Male 41 Fungal culture Sporothrical arthritis S. schenckii Sporothrix spp. [25]
California 1 Female 35 Fungal culture Disseminated S. schenckii Sporothrix spp. [26]
Nebraska 1 Male 62 Fungal culture
Biopsy (Histopathology)
Disseminated S. schenckii Sporothrix spp. [27]
Boston 1 Female 35 MALDI-TOF Fixed cutaneous S. schenckii S. schenckii [28]
Kansas 1 Male 30 Fungal culture
Biopsy (Histopathology)
Disseminated S. schenckii Sporothrix spp. [29]
Florida 1 Male 76 History and physical examination Lymphocutaneous Sporothrix spp. Sporothrix spp. [30]
Oklahoma 1 Male 23 Fungal culture Lymphocutaneous S. schenckii complex Sporothrix spp. [31]
Washington 1 Female 44 Fungal culture
PCR sequencing (ITS 1–2)
Disseminated S. schenckii S. schenckii [32]
Arizona 1 Female 72 PCR DNA sequencing Laryngotracheal granulomatous disease S. schenckii S. schenckii [33]
Mexico Veracruz 1 Male 39 Fungal culture
Biopsy (Histopathology)
Atypical S. schenckii Sporothrix spp. [34]
Puebla 1 Male 36 Fungal culture
Biopsy (Histopathology)
Disseminated S. schenckii Sporothrix spp. [35]
Oaxaca 1 Male 13 Fungal culture Lymphocutaneous on the left hand, forearm, and upper arm Sporothrix spp. Sporothrix spp. [36]
Mexico City 1 Male 54 Fungal culture
Biopsy (Histopathology)
Disseminated (Testicular involvement) S. schenckii Sporothrix spp. [37]
Guerrero 1 Female 36 Fungal culture
Biopsy (Histopathology)
Disseminated Sporothrix spp. Sporothrix spp. [38]
Durango 1 Male 68 Fungal culture
Biopsy (Histopathology)
Disseminated Sporothrix spp. Sporothrix spp. [39]
ND 24 Male
(16)
Female
(8)
Average: 35.5 PCR sequencing (calmodulin gene) Cutaneous disseminated
16 (66.7%)
Cutaneous disseminated + Mucosal
3 (12.5%)
Joint
1 (4.1%)
Visceral
1 (4.1%)
Fungaemia
1 (4.1%)
Mucosal + Visceral + Fungemia:
1 (4.1%)
Visceral + Fungaemia
1 (4.1%)
S. schenckii
23 (95.5%).
S. globosa
1 (4.5%)
S. schenckii
23 (95.5%).
S. globosa
1 (4.5%)
[40]
ND 55 Male
(34)
ND
Female
(18)
  Sporotrichin Skin Test
Fungal culture
Lymphocutaneous 32 (58.2%)
Fixed cutaneous
19 (34.5%)
Disseminated
4 (7.3%)
S. schenckii
54 (98%)
S. globosa
1 (2%)
S. schenckii
54 (98%)
S. globosa
1 (2%)
[41]
Guerrero 73 Male
(33)
Female
(40)
Average: 25.8 Fungal culture
Biopsy (Histopathology)
Lymphocutaneous: 41 (56.16%)
Fixed cutaneous
24 (32.87%)
Disseminated
8 (10.95%)
S. schenckii S. schenckii [42]
Chihuahua 1 Female 84 Multiplex PCR (Calmodulin gene) Fixed cutaneous (Auricular sporotrichosis) S. schenckii (sensu stricto) S. schenckii [43]
Baja California 1 Male 23 Fungal culture
Biopsy (Histopathology)
Lymphocutaneous S. schenckii Sporothrix spp. [44]
San Luis Potosi 8
Puebla 3
Mexico City 2
Queretaro 2
Guanajuato 2
Jalisco 1
Zacatecas 1
Michoacan 1
Morelos 1
State of Mexico 1
22 ND   PCR sequencing (Calmodulin and calcium-calmodulin-dependent kinase genes) Lymphocutaneous: 17 (77.3%)
Fixed cutaneous
4 (18.2%)
Disseminated
1 (4.5%)
S. schenckii:
18 (81.8%)
S. globosa
4 (18.2%)
S. schenckii:
18 (81.8%)
S. globosa
4 (18.2%)
[45]
Puebla 4
Nuevo Leon 2
Oaxaca 6
Mexico City 3
Jalisco 2
17 ND   PCR sequencing (Calmodulin gene) Lymphocutaneous: 16 (94.11%)
Disseminated: 1 (5.88%)
S. schenckii:
16 (94.11%)
S. globosa
1 (5.88%)
S. schenckii:
16 (94.11%)
S. globosa
1 (5.88%)
[46]
Guerrero 76 Male (35)
Female
(41)
<18: 37
>18: 39
Fungal culture
Biopsy (Histopathology)
Lymphocutaneous 43 (56.8%)
Fixed cutaneous
24 (32.3%)
Disseminated
8 (11%)
Sporothrix spp. Sporothrix spp. [47]
Jalisco 1057
Nayarit 23
Zacatecas 20
Michoacan 19
Guanajuato 12
Veracruz 1
Chihuahua 1
1134 Male
(669)
Female
(465)
  ND Lymphocutaneous: 782 (69%)
Fixed cutaneous:
308 (27.2%)
Disseminated
44 (38.8%)
S. schenckii complex Sporothrix spp. [48]
ND 1 Male 45 PCR sequencing (Calmodulin gene) Disseminated S. schenckii complex S. schenckii [49]
ND 1 Male 56 Fungal Culture
Biopsy (Histopathology)
PCR sequencing (ITS and calmodulin gene)
Fixed cutaneous sporotrichosis S. mexicana S. mexicana [50]
ND 18 Male
(10)
Female
(8)
ND PCR sequencing (ITS regions) Lymphocutaneous 13 (72.2%)
Fixed cutaneous
5 (27.8%)
S. schenckii
17 (94.4%)
S. globosa: 1 (5.6%)
S. schenckii
17 (94.4%)
S. globosa: 1 (5.6%)
[51]
Oaxaca 2 Male 61 Multiplex PCR (Calmodulin gene) Fixed cutaneous
1 (50%)
Disseminated
1 (50%)
S. schenckii sensu stricto S. schenckii [52]
Male 21
ND: Not Determined.

3. Epidemiology of Sporotrichosis in Central America and the Caribbean

Only 8 publications with 126 cases of sporotrichosis were found in Central America and the Caribbean [53,54,55,56,57,58,59,60]. In the only article found from Costa Rica during the search period, 57 isolates were analyzed in San José, finding the presence of 2 species: S. schenckii sensu stricto (93%), S. brasiliensis (3.5%), and Sporothix spp. (3.5%) [53]. On the other hand, there were 3 reports in Guatemala with 65 cases (98.5% Sporothrix spp. and 1.5% S. schenckii sensu stricto), with all cases being from Guatemala City [54,55,56]. Finally, reports of a single case were found in Honduras (Tegucigalpa); the agent responsible for the infection was S. schenckii, and in Panama (Correa District), the agent was not determined [57,58]. In the Caribbean, only two reports of S. schenckii sensu lato from Cuba were found [59,60]. Regarding the new taxonomic classification, it was determined that in Costa Rica, 93% of the cases were caused by S. schenckii, 3.5% by S. brasiliensis, and 3.5% by Sporothix spp. [53]. Meanwhile, in Guatemala, the main pathogenic agent was Sporothrix spp. with 98.5% and S. schenckii with 1.5% [54,55,56]. In Honduras and Panama, it was observed that the agent Sporothrix spp. was responsible for sporotrichosis, with one case per country (100%) [57,58]. In Cuba, there were two reports of a case due to Sporothrix spp., which represents 100% [59,60].
The most frequently reported form was lymphocutaneous with 39 cases (30.95%), followed by fixed cutaneous with 26 (20.63%), the disseminated form with 2 (1.59%), 1 case of chancre (0.79%), and 58 ND cases (46.03%) [53,54,55,56,57,58,59,60]. The most common etiological agents noted were Sporothrix spp. with 55.56% (70/126), S. schenckii with 42.85% (54/126), and S. brasiliensis with 1.59% (2/126) [53,54,55,56,57,58,59,60].
Regarding diagnosis, fungal culture was used as a diagnostic method in all articles (8/8), followed by histopathological examination (5/8). In this case, also, the histopathological examination was always accompanied by fungal cultures. PCR sequencing (2/8) employing the calmodulin gene in one article and the ITS1-2 region in the other was also used as a diagnostic tool. Lastly, diagnosis with microscopy using lactophenol blue was mentioned in two reports (Table 2) [53,54,55,56,57,58,59,60].
Table 2. Epidemiology of Sporotrichosis in Central America and the Caribbean.
Region Country City Number of Reported Cases Vulnerable Population Diagnostic Method Type of Sporotrichosis Etiological Agents
(%)
References
Sex Age (Years) Taxonomy
Before 2017 After 2017
Central America Costa Rica San José 57
(1994–2015)
No data   Direct microscopy, culture, PCR (enzymatic restriction and sequencing of the calmodulin gen) ND S. schenckii sensu stricto
53 (93%)
S. brasiliensis
2 (3.5%)
Sporothrix spp.
2 (3.5%)
S. schenckii
53 (93%)
S. brasiliensis
2 (3.5%)
Sporothrix spp.
2 (3.5%)
[53]
Guatemala Guatemala City 11 Male 7
Female 4
Average 49 years Fungal culture,
Histopathology
Fixed cutaneous
9 (81.8%)
Lymphocutaneous
2 (18.2%)
Sporothrix spp. (100%) Sporothrix spp. (100%) [54]
Guatemala City 53
(2007–2016)
Male 33
Female 20
Average 44.1 years Fungal culture,
microscope with Lactophenol
cotton blue
Lymphocutaneous 33 (62.2%)
Fixed cutaneous
17 (32.1%)
Disseminated
2 (3.8%)
Chancre
1 (1.9%)
Sporothrix schenckii complex.
(100%)
Sporothrix spp.
(100%)
[55]
Guatemala City 1 ND   Fungal culture, PCR sequencing (ITS 1- 2 and β
-tubulin)
ND Sporothrix schenckii sensu stricto Sporothrix schenckii [56]
Honduras Tegucigalpa 1 Male 1 14 years Fungal culture Lymphocutaneous
1 (100%)
S. schenckii Sporothrix spp. [57]
Panamá Chorrera District 1 Male 1 34 years Clinical,
Direct Microscopy, Fungal culture.
Lymphocutaneous
1 (100%)
ND Sporothrix spp. [58]
Caribbean Cuba Pinar del Río 1 Female 1 57 years Histopathology
Fungal culture
Lymphocutaneous Sporothrix schenckii sensu lato
(100%)
Sporothrix spp.
(100%)
[59]
Cumanayagüa 1 Male 67 Histopathology,
Fungal culture,
Microscopy with lactophenol cotton blue
Lymphocutaneous Sporothrix schenckii
sensu lato
(100%)
Sporothrix spp.
(100%)
[60]
ND: Not Determined.

4. Epidemiology of Sporotrichosis in South America

A total of 68 publications with 11,050 cases of sporotrichosis were found in South America [61,62,63,64,65,66,67,68,69,70,71,72,73,74,75,76,77,78,79,80,81,82,83,84,85,86,87,88,89,90,91,92,93,94,95,96,97,98,99,100,101,102,103,104,105,106,107,108,109,110,111,112,113,114,115,116,117,118,119,120,121,122,123,124,125,126,127,128,129,130,131]. Of these, 4 reports were found in Argentina during the analyzed period with 38 cases, of which 9 were caused by S. schenckii sensu stricto (23.68%), 26 by S. brasiliensis (68.52%), 1 by S. globosa (2.6%), 1 by S. schenckii (2.6%), and 1 by S. schenckii complex (2.6%) [61,62,63,64]. Brazil reported 42 articles with 5546 analyzed cases [65,66,67,68,69,70,71,72,73,74,75,76,77,78,79,80,81,82,83,84,85,86,87,88,89,90,91,92,93,94,95,96,97,98,99,100,101,102,103,104,105,106], identifying Sporothrix spp. and S. schenckii complex as the causative agent in 4906 cases (88.46%), S. schenckii in 302 (5.45%), S. brasiliensis in 125 (2.25%), Sporothrix sensu lato in 110 (1.98%), S. globosa plus S. schenckii in 91 cases (1.64%) Sporothrix sensu stricto in 5 (0.09%), S. globosa in 4 (0.07%), and S. mexicana in 3 (0.05%) during the studied period. In Colombia, 4 reports were found, adding up to 50 cases [56,107,108,109].S. Schenckii sensu stricto was identified in 22 cases (44.00%), Sporothrix spp. in 15 (30.00%), S. globosa in 12 (24.00%) and S. schenckii sensu lato in 1 (2.00%). Likewise, in Chile, 3 reported cases detected Sporothrix spp. in 1 (33.33%), S. globosa in 1 (33,33%), and Sporothrix pallida in 1 (33.33%) [110,111,112]. A total of 13 cases of Sporothrix spp. and S. schenckii complex (100%) were reported in Paraguay [113,114]. In Peru, from 4792 cases, S. schenckii was found in 4656 (97.16%), Sporothrix spp. and the Sporothrix complex in 116 (2.42%), S. schenkii sensu stricto in 19 (0.40%), and Sporothrix sensu lato in 1 (0.02%) [115,116,117,118,119,120,121,122,123]. There was 1 report of 157 cases of Sporothrix spp. (100%) found in Uruguay [124]. Finally, there were 4 reports from Venezuela with 452 cases of Sporothrix spp., and the Sporothrix complex was found in 220 of those cases (48.67%), S. schenckii sensu lato in 130 (28.76%), S. schenckii in 42 (9.29%), S. schenckii sensu stricto in 17 (3.76%), S. globosa in 39 (8.63%), 1 case of Ophiostoma stenoceras (0.22%) and 3 cases were ND (0.66%) [125,126,127,128].
Regarding the new taxonomic classification, in Argentina, 26.31% were S. schenckii, 68.42% S. brasiliensis, 2.63% S. globosa, and 2.63% Sporothrix spp. [61,62,63,64]. In Brazil, the main pathogenic agent was Sporothrix spp. with 95.56%, S. brasiliensis 2.25%, S. globosa plus S. schenckii 1.64%, S. schenckii 0.41%, S. globosa 0.07%, and S. mexicana 0.05% [65,66,67,68,69,70,71,72,73,74,75,76,77,78,79,80,81,82,83,84,85,86,87,88,89,90,91,92,93,94,95,96,97,98,99,100,101,102,103,104,105,106]. In Colombia, S. schenckii 44.00%, Sporothrix spp. 32.00%, and S. globosa 24.00% were the principal mycotic agents [56,107,108,109]. Regarding Chile, the pathogenic agents were Sporothrix spp., S. globose, and S. pallida (33.33% each) [110,111,112]. In Paraguay, the unique agent found was Sporothrix spp. (100%) [113,114]. For Peru, the most important pathogenic agents were Sporothrix spp. (99.54%), and S. schenckii (0.46%) [115,116,117,118,119,120,121,122,123]. In Uruguay, 100% of the cases were due to Sporothrix spp. (100%) [124]. In Venezuela, Sporothrix spp. (80.04%), S. schenckii (13.38%), and S. globose (6.57%) were the types of Sporothrix agents [125,126,127,128].
The most frequent types of disease were lymphocutaneous with 3293 cases (29.47%), fixed cutaneous with 1947 (17.43%), disseminated cutaneous with 34 (0.30%), systemic form with 18 (0.16%), and others with 177 cases (1.60%). However, there were 5702 cases (51.04%) with undetermined types from all the cases diagnosed as sporotrichosis [56,61,62,63,64,65,66,67,68,69,70,71,72,73,74,75,76,77,78,79,80,81,82,83,84,85,86,87,88,89,90,91,92,93,94,95,96,97,98,99,100,101,102,103,104,105,106,107,108,109,110,111,112,113,114,115,116,117,118,119,120,121,122,123,124,125,126,127,128].
The most common reported etiological agent with the new taxonomical classification was Sporothrix spp. with 95.12% (10,511/11,050), followed by S. schenckii with 1.23% (136/11,050), S. brasiliensis with 2.27% (251/11,050), S. globosa plus S. schenckii with 0.82% (91/11,050), S. globosa with 0.52% (57/11,050), S. mexicana 0.027% (3/11,050), and S. pallida with 0.009% (1/11,050) [56,61,62,63,64,65,66,67,68,69,70,71,72,73,74,75,76,77,78,79,80,81,82,83,84,85,86,87,88,89,90,91,92,93,94,95,96,97,98,99,100,101,102,103,104,105,106,107,108,109,110,111,112,113,114,115,116,117,118,119,120].

This entry is adapted from the peer-reviewed paper 10.3390/jof8060588

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