Next Article in Journal
Market Participation and Farmers’ Adoption of Green Control Techniques: Evidence from China
Previous Article in Journal
Biological Control Options for the Management of Tadpole Shrimp (Triops longicaudatus (LeConte)) in California Rice
 
 
Search for Articles:
Title / Keyword
Author / Affiliation / Email
Journal
Article Type
 
 
Advanced Search
 
Section
Special Issue
Volume
Issue
Number
Page
 
Journals
Agriculture
Volume 14
Issue 7
10.3390/agriculture14071137
agriculture-logo
Submit to this Journal Review for this Journal Propose a Special Issue
► Article Menu

Article Menu

share Share announcement Help format_quote Cite question_answer Discuss in SciProfiles thumb_up
...
Endorse textsms
...
Comment
first_page
settings
Order Article Reprints
Font Type:
Arial Georgia Verdana
Font Size:
Aa Aa Aa
Line Spacing:
Column Width:
Background:
Review

Incidence of Photosensitization in Husbandry Animals: A Meta-Study on the Effects of Feed Diversity and Feed Choice

by
Rieke Moritz
and
Sabine Aboling
*
Institute of Animal Nutrition, University of Veterinary Medicine, Hannover, Foundation, Bischofsholer Damm 15, 30173 Hannover, Germany
*
Author to whom correspondence should be addressed.
Agriculture 2024, 14(7), 1137; https://doi.org/10.3390/agriculture14071137
Submission received: 28 May 2024 / Revised: 8 July 2024 / Accepted: 9 July 2024 / Published: 13 July 2024
(This article belongs to the Section Farm Animal Production)
Browse Figures
Versions Notes

Abstract

:
As this is a meta-study, we examined whether plant species diversity in the feed and the possibility of feed choice would influence the number of cases of photosensitization in farm animals. We evaluated 110 scientific references which described 172 cases of photosensitization worldwide, mainly in husbandry animals between 1926 and 2022. More than 50% of the cases occurred in South America and Australia. Among the animal species, sheep and cattle were statistically overrepresented. A total of 35 organisms were revealed to be phototoxic: 24 herbs, 2 grasses, 7 woody species, and 2 kinds of fungi. Animals developed mainly secondary photosensitization due to fresh feed (71.8%) of normal quality (88.1%), indicating that the phototoxic agents are from liver-toxic plants such as the grass Brachiaria and the herb Froelichia. Horses fell ill chiefly with primary photosensitization due to directly acting phototoxic agents of plant species such as the herbs Medicago and Pastinaca, both in fresh and conserved feed. Goats manage to avoid phototoxic plants under both high and low feed diversity if they still have free choice between plant species. High feed diversity reduced the incidence 2.4-fold, while enabled selection possibility even reduced it 7.5-fold. Since the lack of choice between forage plants was revealed to be the main cause of photosensitization, this knowledge could be used to prevent the disease in livestock.

1. Introduction

Cases of plant poisoning in animals are not easy to verify by tracing them back to plants because the symptoms are either unspecific [1], subtle [2], or the suspicious plants ingested are simply not visible any more [3]. Moreover, signs of grazing are inconspicuous and thus often overlooked [4]. One exception in plant poisoning is photosensitization, caused by some 250 phototoxic plant species worldwide [5] and the fungus Pithomyces chartarum [6]. The alimentary-induced disease is manifested in four variants, primary, secondary, endogenous, and idiopathic photosensitization [7,8] while Pithomyces causes exclusively secondary photosensitization [9]. In any case, symptoms are external, prominent, and resemble human photodermatitis (“sunburn”). This might be the reason why these organisms are generally well-known to animal keepers too. Although photosensitization can be confused with similar-looking contact eczema, a differential diagnosis is facilitated if phototoxic plant species (or fungi) appear between (or on) feed stuff or in pastures. Moreover, an unambiguous classification system of photosensitization is available [7,8]. Prominent examples of phototoxic plants are the genera Heracleum and Hypericum. Their compounds coumarin and hypericin accumulate in the skin and interact with sunlight, causing primary phototoxicity on the skin [10,11]. Except in a few cases in birds, white-colored mammals are most often affected, although symptoms can be observed in all kinds of colored mammals. Since the etiology of plant-born photosensitization is well-known, so are the phototoxic plant species [5]. The question therefore arose as to why farm animals are still being poisoned with phototoxic plants. This question is of special interest since in times of global change the incidence of this disease might be increase [12]. Here, we address the two key variables concerned with plant poisoning of husbandry animals in general [13]: (1) the extent of possibility of feed choice, and (2) the number of plant species in the feed, the so-called α-diversity [14]. Both variables have been widely discussed with regard to animal welfare [15] and nutritional ecology [16,17,18]; however, in the modern farm feeding regime [19] they are neglected [15]. The goal of this meta-study was to investigate whether the level of plant diversity in the feed or the extent of feed choice influences the number of cases of photosensitization in farm animals.

2. Materials and Methods

2.1. Search for Case Reports

We reviewed references of reported cases of photosensitization caused by potential phototoxic organisms from as early as 1926 up to today, using electronic databases such as Web of Science, CAB Abstracts, and VetSearch. Among the publication formats there were case reports, brief communications, and reviews, independent of being peer-reviewed or not. To ensure we could rely on the data, both the material and methods of the evaluated references were checked. We distinguished, too, whether the author proved or only suspected a connection with a certain phototoxic organism. In addition, the author’s indication of the phototoxic potential of the organism was checked in a second source. This source was the most modern accessible publication, such as a paper or textbook, that deals with the corresponding chemistry and phototoxic agents of the organism mentioned in a case.
Non-German and non-English papers were considered if the English abstract contained the raw data mentioned above. Numerous non-English publications did not present an English abstract and were dismissed. Case collections counted as one case if the data did not allow several cases to be differentiated from each other. If the disease was a secondary finding of studies with another research focus (e.g., [20]), it counted as a case as well. However, experimentally induced photosensitization was excluded. Furthermore, publications with a non-alimentary background for hepatogenous photosensitization, such as liver-migrating endoparasites (e.g., [21]), were not part of this meta-study.

2.2. Variables of Evaluation Case Reports

Along with certain raw data selected from the references, such as the kind of phototoxic organism or the kind of feed, additional data were extracted from the sources such as α-diversity and feed quality that were not explicitly addressed by the authors but mentioned anyway. In total, the cases of photosensitization evaluated included the following seven principal variables along with the two key variables: (1) level of feed examination, (2) kind of phototoxic organism, (3) type of photosensitization, (4) animal species, (5) kind and quality of feed, (6) plant species diversity of feed (first key variable), and (7) possibility of feed choice (second key variable; Figure 1).

2.2.1. Level of Feed Examination

The first principal variable “level of feed examination” was determined by asking if the authors examined the quality and botanical composition of the feed (1) completely, (2), partly, or (3) whether it was unknown.
The feed was considered as completely examined if the authors (a) inspected the pasture and indicated the presence of plant species other than the already identified phototoxic ones, (b) stated that no other phototoxic plants were growing there, (c) noted that a phototoxic plant species was found in large quantities, (d) counted fungi spores in the feed (e.g., [22]), (e) analyzed the feed botanically, (f) stated that no phototoxic plants were found, or (g) named both main plant species and those with a mass portion of less than 5%.
The feed was taken as partly examined if authors (a) searched for the presence or absence of phototoxic plants, (b) stated simply that no other phototoxic plants were present, and (c) indicated the presence of “many” species with no further information.
On the other hand, if there was no information regarding the level of feed examination in the reviewed references or if the authors gave no hints about feed examination, the level of feed examination was considered unknown.

2.2.2. Kind of Phototoxic Organism

Five kinds of phototoxic organisms, (1) grasses, (2) herbs, (3) woody plants, (4) bacteria and fungi, and (5) unknown organisms, were assessed in this study.

2.2.3. Type of Photosensitization

The third principal variable manifested itself in four types: (1) primary (direct), (2) secondary (hepatogenous), (3) endogenous, and (4) idiopathic type [7,8].
The first type, primary photosensitization, occurs when phototoxic components of plants are taken up through ingestion and arrive in the skin unchanged or through direct skin contact [23]. This kind of the disease appears within hours of the ingestion or contact [23]. In contrast, the delayed onset of the disease in other types makes it more difficult to identify the trigger.
The second type, hepatogenous photosensitization, is a consequence of liver diseases caused through liver-toxic plant components [24] or fungi [25]. The damaged liver can no longer excrete photoactive phylloerythrin, a by-product of bacterial digestion of chlorophyll, through the bile [26]. Instead, it accumulates in blood and skin where it causes a range of typical photosensitization symptoms [2].
The third type, endogenous photosensitization, is a metabolic effect inherited in cattle and therefore was not relevant for this study [27].
The fourth type, idiopathic photosensitization, includes cases in which the cause of the disease is not known so far.

2.2.4. Animal Species

The fourth principal variable concerned all mammal herbivorous animal species that appeared in the references considered.

2.2.5. Kind and Quality of Feed

The kind of feed was expressed as (1) “fresh”, in the case of ingestion of living plants either provided on pasture or after being recently harvested in a manger; (2) “conserved”, in the case of hay, silage, or pellets; (3) “both”, if animals had access to both kinds of feed; and finally, (4) “unknown”, if no information about the kind of feed was given by the authors.
The feed was considered of (1) normal quality if there were neither direct nor indirect hints on quality deficiencies apparent in the reference. In the case of (2) poor quality, the authors stated that there was either (a) Pithomyces chartarum on pasture grass or bacteria and fungi (mold) in conserved feed stuff or (b) moisture in the case of hay, the latter according to the criteria described in [28].

2.2.6. Plant Species Diversity

The sixth principal variable (or first key variable) was related to a feed sample or a pasture and thus represented α-diversity, defined as the number of species within a certain unit [14]. α-diversity in our study comprised three subvariables: (1) high-level diversity, (2) low-level diversity, and (3) no information available.
The feed was assumed to be (1) highly diverse if authors (a) stated that there were various weeds present, or (b) found several plants growing on the property or in conserved feed, or (c) mentioned certain key words such as “native vegetation” or “fallow”, or noted plants that are indicator species for a low soil nitrogen level, which means that the α-diversity on grasslands is higher than on intensively fertilized land [29], or if authors (d) listed at least four plant species without stating that one was dominant, the minimum number of species in species-rich meadows in Middle Europe [30].
Low-level diversity (2) was recognized if (a) the pasture or conserved feed consisted of fewer than four plant species, or (b) conserved or fresh feed was stated by the researchers to be dominated or massively invaded by one plant, or (c) animals received pellets only.
In the case of (3) no information available, the authors did not mention any details on botanical α-diversity of feed or pastures.

2.2.7. Possibility of Feed Choice

As for the seventh variable (or second key variable), we discerned three subvariables: (1) feed selection was possible; (2) feed selection was not possible; and (3) feed selection was not known.
Feed selection was considered possible if there were (a) various kinds of feedstuff that were given simultaneously or shortly one after the other, or (b) the pasture or conserved feed possessed a high diversity, as defined in the previous section.
In contrast, feed selection was considered not possible if (a) a pasture was contaminated with fungi such as Pithomyces chartarum, or (b) animals received only pellets, or (c) the pasture vegetation was completely dried out, even if biodiversity was high.
If any relevant information was missing, the possibility for feed selection was regarded as unknown.

2.3. Data Analysis

Most of the data were analyzed descriptively, counting the presence or absence of defined traits corresponding to the above-mentioned variables. In addition, the Pearson correlation coefficient r was calculated using Microsoft Excel© 2013 on the basis of the number of animal nominations for the key variables “plant species diversity of feed” and “possibility of feed choice”. The level of significance was extracted from tables of critical values of the correlation coefficient r in Cann (2004) [31], based on a one-sided test.

3. Results

3.1. Overview of All Variables

The level of feed examination was for the most part either partly or completely carried out (Figure 2). The most abundant kind of phototoxic organism was herbs. Secondary photosensitization turned out to be the predominant type of this disease, with sheep the mainly affected animal species. The feed was largely both of normal quality and fresh. Regarding the key variables, the level of diversity in the feed proved to be mostly low, without the possibility of feed selection.

3.2. Botanical Data Basis

A total of 172 cases of photosensitization were obtained from 110 publications from six continents, mostly from South America (31.4%) (Table 1). Twenty references (18.2%) written in a language other than English but with an abstract in English were evaluated in this study.
The authors mainly fulfilled the precondition for an estimation of diversity because the feed was completely (41.9%) and partly (39.0%) examined botanically, whereas only in a minority of cases it remained unknown (19.2%).
A total of 43 out of 110 references and thus 82 out of 172 cases (39% and 47.6%) were peer-reviewed, while in the rest (61% and 52.3%) this remained unknown (Figure 3).
Apart from 14 cases of idiopathic photosensitization (8.1%), there were 33 cases (19.2%) in which the authors failed to prove the phototoxic agent. In only 5 cases (2.9%) the data were not evidence-based, and concerned cyanobacteria (3 cases) as well as a grass and a herb (1 case each). As for the cyanobacteria, no evidence of their phototoxicity was provided according to a review article [32]. As for the grass (Alopecurus), it was rather a plant-colonizing fungus that was the causative organism according to [33]. As for the herb (Ranunculus), its blister-generating compounds [34] probably caused symptoms of contact dermatitis that strongly resembles photosensitization.

3.3. Phototoxic Organisms

Herbs turned out to be the largest class of phototoxic organisms. In total, 35 phototoxic organisms were involved in the 172 cases. The most frequent phototoxic organism was signal grass (Brachiaria decumbens, Poaceae, 15 cases), followed by the herbaceous cottonweed (Chamaecrista, Fabaceae, 13 cases). Represented by 24 genera (Froelichia, Chamaecrista, Medicago, Tribulus, Hypericum, Biserrula, Pastinaca, Ammi, Brassica, Trifolium, Lotus, Narthecium, Senecio, Cynoglossum, Heliotropium, Persicaria, Alternanthera, Crotalaria, Erodium, Lantana, Petroselinum, Heracleum, Tanacetum, and Thamnosma), herbs were the most diverse functional group among phototoxic organisms and made up the largest proportion of case reports with 106 cases (Figure 4).
There were seven woody plants (Enterolobium, Myoporum, Stryphnodendron, Heterophyllaea, Holocalyx, Malachra, and Phytolacca) that caused 16 cases, and only two grasses (Brachiaria and Panicum) that were involved in 25 cases. Pithomyces chartarum and mold species caused about 12 cases.

3.4. Animal Species, General Feed Characteristics, and Type of Photosensitization

Sheep (n = 69 animals) and cattle (n = 55) accounted for most cases (39.0% and 31.1%; Table 2) because they are commonly kept in large flocks [11] and thus were statistically overrepresented here. Animals received more feed of normal quality (89.3%) than of poor quality (10.7%).
As known from earlier studies (for example [39]), secondary photosensitization happens more frequently (55.4% versus 33.3%; Table 3), with liver-toxic plants as the cause of the disease. In horses, however, the incidence of primary photosensitization was revealed to be higher (18 versus 10 animals).
Fresh feed represented the largest portion among the kinds of feed stuff (Table 4). Most of affected animal individuals (71.8%) went back to fresh feed consisting of whole plants with their complete composition and concentration of secondary metabolites. The few existing cases related to conserved feed (n = 25; 14.1%) may be attributed to phototoxic compounds still being present, yet these are at least partly decomposed during any conservation process. For example Araya and Ford (1981) showed that 80% of the hypericin content was lost when St. John’s Wort (Hypericum perforatum) was dried in the sun [40]. This had been shown for the coumarins in Pastinaca [41] and an unknown component in Medicago [42] too.

3.5. Feed Diversity and Feed Choice

Freshly harvested or still growing phototoxic plants are more effective (n = 127) than their dried or conserved counterparts (n = 25; Table 5), a finding confirmed by [43].
High feed diversity reduced the incidence 2.4-fold (32 versus 77 animals) while selection possibility even reduced it 7.5-fold (15 versus 113 animals), confirming that “selection behaviour has such high importance for the cognitive well-being of ruminants and access to feed diversity should be a compulsory criterion of welfare” [44]. In this context, it was interesting that goats were the only species that did not fall ill if they had any choice to select plant species (incidence = 0) (Table 6).
The incidence of photosensitization in the case of fresh feed was 10-fold lower if selection was possible (8 versus 83 animals; see Table 5), but only 2.6-fold lower in the case of high diversity (21 versus 56 animals). Even in conserved feed, the higher ranking of feed choice was eminent: the incidence of photosensitization in the case of conserved feed was 7.3-fold lower if selection was possible (3 versus 22 animals; see Table 5), but only 2.4-fold lower in the case of high diversity (5 versus 12 animals).

4. Discussion

The introduction of two key variables served to analyze whether the number of photosensitization cases in farm animals was associated with different levels of feed plant diversity or feed choice.

4.1. Reliability of Meta-Data

The high proportion (60.9%) of references without any indication as to whether they are peer-reviewed reflects the small publication format in which case reports often appear, in particular when written decades ago. At 38.4% and 27.7%, the level of diversity and the possibility of feed choice are unknown to a significant extent. However, authors of studies that did not address these variables are not expected to have considered them relevant, probably because the feed lacks a certain species diversity or the animals were not given any feed choice. Otherwise, both variables would have been a significant observation, since dealing with phototoxic organisms presumes that the authors thoroughly look at the feed composition and choice. In conclusion, it is unlikely that unknown feed diversity and choice could be cases of high diversity or selection possibility. The data gap would rather lead to an underestimation of the effects of the two key variables. On the other hand, it was necessary to rely on the authors’ statements on diversity and choice, expressed as indirect parameters. This method might be of varying accuracy and thus could weaken the results presented here.

4.2. Impact of Feed Diversity and Feed Choice on the Incidence of Photosensitization

Since only cases of disease are described in case reports, cases of healthy animals are usually missing. In other words: in our meta-study dealing only with case reports, the incidence is at least n = 1, whereas the number of control individuals is almost always n = 0. Within this database, even optimal conditions such as good quality feed with a high α-diversity and free choice lead to cases of photosensitization. With this bias, the impact of both key variables needs to be discussed. For example, there is an increased probability of the presence of poisonous plants with increasing diversity [45]. Therefore, in feeds of high α-diversity, the frequency of encounters between phototoxic plants and farm animals is increased. On the other hand, even a high diversity is prone to decrease over time under constricted conditions such as overgrazing or lack of ad libitum feeding. At this point, “plant species diversity” implies “dietary choice”. Such a chronological effect of the two paired key variables might be the reason why feed diversity alone diminishes the incidence of photosensitization to a far lesser degree than selection possibility does. Against this background, feed condition plays an essential role. One would suggest that the animals would recognize the respective toxins as repellents in fresh plants and thus would refrain from eating certain species, as anticipated by Provenza et al. (1992) who assumed that an animal is capable of avoiding phototoxic plant species [46]. The tenfold lower incidence of cases in which fresh feed was eaten than in cases of preserved feed shows that successful negative selection indeed occurs, provided that the animals have a choice between feedstuffs or feed plants. α-diversity, an elementary condition for resilient grassland communities [47], is thus favorable for commercial animal nutrition as long as it is accompanied by feeding management with the possibility of feed selection.
The most interesting examples in this context are horses and goats. Horses mainly suffer from primary photosensitization because, more often than other animal species, they receive certain feed plants such as alfalfa (Medicago) or come into contact with weeds such as parsnip (Pastinaca) that cause this kind of photosensitization ([41,42], Appendix A). However, horses fall ill almost regardless of whether the feed is species-rich or not. This could mean that the choice between plants of an initially species-rich feedstuff becomes smaller over the feeding time, resulting in the dominance of phototoxic plants that no longer can be avoided. Such a situation could occur if the feed is not given ad libitum, as is usual in horse racing stables. Moreover, horses might be forced to feed on pure lucerne, a common feedstuff, dried or fresh, for horses kept for pleasure [42,48,49]. Alfalfa is known to cause photosensitization under conditions that have not yet been fully clarified [42]. In both scenarios (no ad libitum or pure alfalfa feeding), horses cannot avoid even brief physical contact with plants with phototoxic agents relevant to the type of primary photosensitization that goes back to direct skin contact of the agents [50,51]. In contrast, goats are tolerant of giant hogweed (Heracleum mantegazzianum), one of the most potent phototoxic plant species [52]. Moreover, according to the data here, goats manage to avoid phototoxic plants under both high and low feed diversity if they still have free choice between plant species. The finding of zero incidence in a genuine database of cases of photosensitization in an animal species known for its selective feeding behavior [53] is remarkable and underlines that feed choice is the ultimate condition for the preservation of animal health.

5. Conclusions

The results of the present meta-analysis indicate that feed choice and diversity are positively related to photosensitization. In particular, animals having low or no possibility of feed choice are more likely to be affected by photosensitization. Therefore, various kinds of feedstuff given simultaneously or the permanent existence of feed plant diversity in the pasture or in the feed trough may prevent photosensitization in farm animals.

Author Contributions

Conceptualization, R.M. and S.A.; methodology, R.M.; software, S.A. and R.M.; validation, R.M. and S.A.; formal analysis, R.M. and S.A; investigation, R.M.; resources, R.M.; data curation, R.M. and S.A.; writing—original draft preparation, R.M. and S.A.; writing—review and editing, R.M. and S.A.; visualization, S.A.; supervision, S.A.; project administration, S.A.; funding acquisition, S.A. All authors have read and agreed to the published version of the manuscript.

Funding

We acknowledge financial support by the Open Access Publication Fund of the University of Veterinary Medicine Hannover, Foundation.

Institutional Review Board Statement

Not applicable.

Data Availability Statement

Data are contained within the article.

Acknowledgments

We thank Bernd Reckels for his administration, Konstanze Friedrich for helping with a translation problem as well as Jana Höner for the opportunity to study a case of photosensitization in her horses that fully recovered.

Conflicts of Interest

The authors declare no conflicts of interest.

Appendix A. Reference List of Case Reports Sorted by Animal Species

  • Cattle
  • Bourke, C.A.; Rayward, D. Photosensitisation in dairy cattle grazing alligator weed (Alternanthera philoxeroides) infested pastures. Aust. Vet. J. 2003, 81, 361–362, doi:10.1111/j.1751-0813.2003.tb11515.x.
  • Cardona-Álvarez, J.; Vargas-Vilória, M.; Paredes-Herbach, E. Clinical and histopathological study of the phototoxic dermatitis in Zebu calves in grazing of Brachiaria decumbens. Revista MVZ Córdoba 2016, 21, 5366–5380, doi:10.21897/rmvz.603.
  • Casteel, S.W.; Weaver, A.D.; Mills, L.L.; Pace, L.W.; Rottinghaus, G.E.; Smith, K.M. Photosensitization outbreak in shorthorn calves in Missouri. J. Vet. Diagn. Invest. 1991, 3, 180–182, doi:10.1177/104063879100300218.
  • Collett, M.G.; Thompson, K.G.; Christie, R.J. Photosensitisation, crystal-associated cholangiohepatopathy, and acute renal tubular necrosis in calves following ingestion of Phytolacca octandra (inkweed). N. Z. Vet. J. 2011, 59, 147–152, doi:10.1080/00480169.2011.567966.
  • Collett, M.G. Bile duct lesions associated with turnip (Brassica rapa) photosensitization compared with those due to sporidesmin toxicosis in dairy cows. Vet. Pathol. 2014, 51, 986–991, doi:10.1177/0300985813513042.
  • M. G. Collett; Z. Matthews. Photosensitivity in Cattle Grazing Brassica Crops. Institute of Veterinary, Animal, and Biomedical Sciences, Massey University, Palmerston North, New Zealand 2015.
  • Davis, A.J.; Collett, M.G.; Steyl, J.C.A.; Myburgh, J.G. Hepatogenous photosensitisation in cows grazing turnips (Brassica rapa) in South Africa. J. S. Afr. Vet. Assoc. 2021, 92, e1-e6, doi:10.4102/jsava.v92i0.2106.
  • Del Méndez, M.C.; Riet-Correa, F.; Schild, A.L.; Ferreira, J.L.; Pimentel, M.A. Fotossensibilizaçäo em bovinos causada por Ammi majus (Umbelliferae) no Rio Grande do Sul. Pesqui. vet. bras 1991, 17–19.
  • Dorsch, M.A.; Cantón, G.J.; Odriozola, E.R. Fotosensibilización primaria por consumo de Ammi majus en bovinos: primer reporte en Argentina. Rev. vet. 2018, 29, 137, doi:10.30972/vet.2923280.
  • Eyged, M.N.; Shlosberg, A.; Eilat, A.; Cohen, U.; Beemer, A. Photosensitization in dairy cattle associated with the ingestion of Ammi majus. Refuah Veterinarith 1974, 31.
  • Glenn, B.L.; Monlux, A.W.; Panciera, R.J. A Hepatogenous Photosensitivity Disease of Cattle: I. Experimental Production and Clinical Aspects of the Disease. Pathologia veterinaria 1964, 1, 469–484, doi:10.1177/030098586400100601.
  • Giaretta, P.R.; Panziera, W.; Galiza, G.J.; Brum, J.S.; Bianchi, R.M.; Hammerschmitt, M.E.; Bazzi, T.; Barros, C.S. Seneciosis in cattle associated with photosensitization. Pesq. Vet. Bras. 2014, 34, 427–432, doi:10.1590/S0100-736X2014000500007.
  • Grecco, F.B.; Dantas, A.F.M.; Riet-Correa, F.; Leite, C.G.D.; Raposo, J.B. Cattle intoxication from Enterolobium contortisiliquum pods. Vet. Hum. Toxicol. 2002, 44, 160–162.
  • Horn, G.A.; Burrows, G.E. Primary photosensitization in cattle. Vet. Hum. Toxicol. 1990, 32, 331–332.
  • House, J.K.; George, L.W.; Oslund, K.L.; Galey, F.D.; Stannard, A.W.; Koch, L.M. Primary photosensitization related to ingestion of alfalfa silage by cattle. J. Am. Vet. Med. Assoc. 1996, 209, 1604–1607.
  • Jerrett, I.V.; Chinnock, R.J. Outbreaks of photosensitisation and deaths in cattle due to Myoporum aff. Insulare R. Br. toxicity. Aust. Vet. J. 1983, 60, 183–186, doi:10.1111/j.1751-0813.1983.tb05959.x.
  • Jesse, F.; Ramanoon, S. Hepatogenous Photosensitization in Cattle- A case Report. Vet World 2012, 5, 764, doi:10.5455/vetworld.2012.764-766.
  • Kelch, W.J.; Kerr, L.A.; Adair, H.S.; Boyd, G.D. Suspected buttercup (Ranunculus bulbosus) toxicosis with secondary photosensitization in a Charolais heifer. Veterinary and human toxicology (USA) 1992.
  • Lazaro, N.D.; Bacha, F.B.; Pupin, R.C.; Paula, J.P.L. de; Leal, P.V.; Pott, A.; Gomes, D.C.; Lemos, R.A.A. de. Photosensitization in Cattle Caused by Spontaneous and Experimentally Ingestion of Stryphnodendron fissuratum. Acta Scientiae. Vet. 2018, 46, 8, doi:10.22456/1679-9216.81829.
  • Lugton, I.W.; Woolacott, J. Liver necrosis and photosensitisation in cattle after eating Persicaria lapathifolia (pale knotweed) and Persicaria orientalis (Prince’s feather). Aust. Vet. J. 2014, 92, 62–64, doi:10.1111/avj.12148.
  • McKenzie, R.A.; Dunster, P.J.; Burchill, J.C. Smartweeds (Polygonum spp) and photosensitisation of cattle. Aust. Vet. J. 1988, 65, 128, doi:10.1111/j.1751-0813.1988.tb14432.x.
  • Mendonça, F.; Evencio-Neto, J.; Baratella-Evêncio, L.; Dória, R.; Freitas, S.H.; Pelegrini, L.; Cruz, R.; Ferreira, E.; Colodel, E. Natural and Experimental Poisoning of Cattle by Enterolobium contortisiliquum Pods (Fabaceae Mimosoideae) in Central-Western Brazil. Acta Veterinaria Brno - ACTA VET BRNO 2009, 78, 621–625, doi:10.2754/avb200978040621.
  • Rocha E Silva, M. Photosensitization in Cattle, caused by Holocalyx glaziovii. Arq. Inst. biol. 1940, 11, 461–488.
  • Scruggs, D.W.; Blue, G.K. Toxic hepatopathy and photosensitization in cattle fed moldy alfalfa hay. J. Am. Vet. Med. Assoc. 1994, 204, 264–266.
  • Silva Filho, G.B.; Chaves, H.A.; Albuquerque, R.F.; Souza, P.E.; Vieira, M.E.; Nascimento, A.L.; Lima, S.C.; Mendonça, F.S. Spontaneous and experimental poisoning by Froelichia humboldtiana in cattle. Pesq. Vet. Bras. 2020, 40, 1–6, doi:10.1590/1678-5150-pvb-6351.
  • Souza, P.E.C.; Oliveira, S.S.; Aguiar-Filho, C.R.; Cunha, A.L.B.; Albuquerque, R.F.; Evêncio-Neto, J.; Riet-Correa, F.; Mendonça, F.S. Primary photosensitization in cattle caused by Froelichia humboldtiana. Res. Vet. Sci. 2012, 93, 1337–1340, doi:10.1016/j.rvsc.2012.04.005.
  • Thawait; Kumar, V.; Dixit; A., A.; Maiti; S.K.; Gupta; Rashmi. Berseem induced Photosensitization and its Therapeutic Management in Cattle. INTAS POLIVET 2013, 14, 228–229.
  • Witte, S.T.; Curry, S.L. Hepatogenous photosensitization in cattle fed a grass hay. J. Vet. Diagn. Invest. 1993, 5, 133–136, doi:10.1177/104063879300500135.
2.
Goat
  • Glastonbury, J.R.; Boal, G.K. Geeldikkop in goats. Aust. Vet. J. 1985, 62, 62–63, doi:10.1111/j.1751-0813.1985.tb14238.x.
  • Lemos, R.A.A. de; Nakazato, L.; Herrero Junior, G.O.; Da Silveira, A.C.; Porfírio, L.C. Fotossensibilização e colangiopatia associada a cristais em caprinos mantidos sob pastagens de Brachiaria decumbens no Mato Grosso do Sul. Cienc. Rural 1998, 28, 507–510, doi:10.1590/S0103-84781998000300026.
  • Neves, J.P.L.; Silveira, Ana Eliza dos Santos; Rocha, N.S.; Crocomo, L.F.; Alves, C.E.F.; Ferreira, M.B.; Da Silva, F.G.O.; Filho, W.C.M. PHOTOSENSITIZATION IN A KID GOAT-CASE REPORT/FOTOSSENSIBILIZACAO HEPATOGENA EM CABRITO-RELATO DE CASO/FOTOSENSIBILIZACION HEPATOGENA EN CABRITO-REPORTE DE UN CASO. Veterinaria e Zootecnia 2016, 23, 588.
  • Abas Mazni, O.; Sharif, H.; Mohd; Khusahry and H.N. Vance. Photosensitization in goats grazed on brachiaria decumbens. Available online: http://jtafs.mardi.gov.my/index.php/publication/issues/archive/133-1985/volume-13-no2/1103-130211 (accessed on 9 November 2022).
  • Santos, D.S.; Silva, C.C.B.; Araújo, V.O.; Fátima Souza, M. de; Lacerda-Lucena, P.B.; Simões, S.V.D.; Riet-Correa, F.; Lucena, R.B. Primary photosensitization caused by ingestion of Froelichia humboldtiana by dairy goats. Toxicon 2017, 125, 65–69, doi:10.1016/j.toxicon.2016.11.258.
3.
Horse
  • Aboling, S. (2021). Phototoxis in white skinned horses due to roughage – a case report. Not published.
  • Barbosa, J.D.; Oliveira, C.M.C. de; Tokarnia, C.H.; Peixoto, P.V. Fotossensibilização hepatógena em eqüinos pela ingestão de Brachiaria humidicola (Gramineae) no Estado do Pará. Pesq. Vet. Bras. 2006, 26, 147–153, doi:10.1590/S0100-736X2006000300003.
  • Berry, J.M.; Merriam, J.G. Phototoxic dermatitis in a horse. (A case report). Vet. Med. Small Anim. Clin. 1970, 65, 251–257.
  • Colon, J.L.; Jackson, C.A.; Del Piero, F. Case Presentation: Hepatic Dysfunction and Photodermatitis Secondary to Alsike Clover Poisoning. Compendium on Continuing Education for the Practicing Veterinarian [Online], 1022–1025.
  • Da Trindade Nobre, V.M.; Riet-Correa, F.; Barbosa Filho, J.M.; Dantas, A.F.M.; Tabosa, I.M.; Vasconcelos, J.S. Intoxicação por Crotalaria retusa (Fabaceae) em Eqüídeos no semi-árido da Paraíba. Pesq. Vet. Bras. 2004, 24, 132–143, doi:10.1590/S0100-736X2004000300004.
  • Fincher, M.G.; Fuller, H.K. Photosensitization-Trifoliosis-Light Sensitizacion. Cornell Veterinarian 1942, 32, 95–98.
  • Gava, A.; Barros, C.S. Senecio spp. poisoning of horses in southern brazil. Pesq. Vet. Bras. 1997, 17, 36–40, doi:10.1590/S0100-736X1997000100006.
  • Ivens, P. Hogweed suspected of causing primary photosensitisation in a horse. Vet. Rec. 2011, 169, 81–82, doi:10.1136/vr.d4472.
  • Knight, A.P.; Kimberling, C. V.; Sternitz, F. R.; Roby, M. R. Cynoglossum officinale (hound’s-tongue)--a cause of pyrrolizidine alkaloid poisoning in horses. J. Am. Vet. Med. Assoc. 1984, 185, 647–650.
  • Medeiros, R.M.T.; Bezerra, V.K.D.; Riet-Correa, F. Intoxicação experimental por Froelichia humboldtiana em equinos. Cienc. Rural 2014, 44, 1837–1840, doi:10.1590/0103-8478cr20131417.
  • Mohamed, F.H.A.; Imbabi, S.E.; Adam, S.E.I. Hepatogenous photosensitization in horses due to Aphis craccivora on lucerne. Bulletin of Animal Health and Production in Africa 1977, 25, 184–187.
  • Puschner, B.; Chen, X.; Read, D.; Affolter, V.K. Alfalfa hay induced primary photosensitization in horses. Vet. J. 2016, 211, 32–38, doi:10.1016/j.tvjl.2016.03.004.
  • Renner, J.E.; Gallo, G.G.; Montesinos Ramos, I.G.; Baschlar, H.O. Contact photodermatitis and keratitis in horses due to parsnip. Vet. Arg. 1991, 450–454.
  • Singh, R.P. A case of photosensitisation in horse. Indian Vet. J. 1970, 47, 450–451.
  • Traub, J.L.; Potter, K.A.; Bayly, W.M.; Reed, S.M. Alsike clover poisoning [in a horse]. Modern Veterinary Practice 1982, 63, 307–309.
  • Vind R. A case of hypericin poisoning in a horse. Nordisk Veterinaermedicin 1957, 322–328.
  • Winter, J.C.; Thieme, K.; Eule, J.C.; Saliu, E.-M.; Kershaw, O.; Gehlen, H. Photodermatitis and ocular changes in nine horses after ingestion of wild parsnip (pastinaca sativa). BMC veterinary research 2022, 18, 80, doi:10.1186/s12917-022-03162-2.
4.
Sheep
  • Al-Dujaily, A.H.; Abeed, S.A.; Hatem, A.A. Photosensitation in sheep associated with ingestion of Tribulus Terrestris in Al-Najaf Desert, Iraq. Plant Archives 2019, 19, 280–283.
  • Amjadi, A.R.; Ahourai, P.; Baharsefat, M. First report of Geeldikkop in sheep in Iran. Archives of Razi Institute 1977, 29, doi:10.22092/ari.1977.108807.
  • Araújo, V.O. de; Oliveira Neto, T.S.; Simões, S.V.D.; Da Silva, T.K.F.; Riet-Correa, F.; Lucena, R.B. Primary photosensitization and contact dermatitis caused by Malachra fasciata Jacq. N.V. (Malvaceae) in sheep. Toxicon 2017, 138, 184–187, doi:10.1016/j.toxicon.2017.09.009.
  • Badiei, K.; Mostaghni, K.; Nazifi, S.; Khodakaram Tafti, A.; Ghane, M.; Momeni, S.A. Experimental Panicum miliaceum poisoning in sheep. Small Ruminant Research 2009, 82, 99–104, doi:10.1016/j.smallrumres.2009.02.002.
  • Bourke, C.A. Sunlight associated hyperthermia as a consistent and rapidly developing clinical sign in sheep intoxicated by St John’s wort (Hypericum perforatum). Aust. Vet. J. 2000, 78, 483–488, doi:10.1111/j.1751-0813.2000.tb11868.x.
  • Bridges, C.H.; Camp, B.J.; Livingston, C.W.; Bailey, E.M. Kleingrass (Panicum coloratum L.) poisoning in sheep. Vet. Pathol. 1987, 24, 525–531, doi:10.1177/030098588702400609.
  • Brook, P.J.; Mutch, G.V. Field control of facial eczema of sheep. New Zealand Journal of Agricultural Research 1964, 7, 138–145, doi:10.1080/00288233.1964.10418146.
  • Brum, K.B.; Haraguchi, M.; Lemos, R.A.; Riet-Correa, F.; Fioravanti, M.C.S. Crystal-associated cholangiopathy in sheep grazing Brachiaria decumbens containing the saponin protodioscin. Pesq. Vet. Bras. 2007, 27, 39–42, doi:10.1590/S0100-736X2007000100007.
  • Bull, L.B.; Macindoe, R.H.F. Photosensitization in Sheep: Trefoil Dermatitis. Aust. Vet. J. 1926, 2, 85–91, doi:10.1111/j.1751-0813.1926.tb05332.x.
  • Button, C.; Paynter, D.I.; Shiel, M.J.; Colson, A.R.; Paterson, P.J.; Lyford, R.L. Crystal-associated cholangiohepatopathy and photosensitisation in lambs. Aust. Vet. J. 1987, 64, 176–180, doi:10.1111/j.1751-0813.1987.tb09677.x.
  • Choez A., K.; Galarza Z., P. Brote de jacapo en ovinos en Junín, Perú. Rev. investig. vet. Perú 2018, 29, 1060–1064, doi:10.15381/rivep.v29i3.14839.
  • DENT, C.H.R.; Kater), J.C.R.(A CONDITION RESEMBLING FACIAL ECZEMA IN SHEEP IN NEW SOUTH WALES. Aust. Vet. J. 1967, 43, 71, doi:10.1111/j.1751-0813.1967.tb15072.x.
  • Diamantino, G.M.L.; Pierezan, F.; Ferreira, M.I.C.; Rocha, W.S.D.; Veiga, V.M.O.; Martins, C.E.; Veiga, M.O.; Soto-Blanco, B. Photosensitization by Brachiaria ruziziensis in a sheep herd. Toxicon 2020, 185, 1–4, doi:10.1016/j.toxicon.2020.06.022.
  • Faccin, T.C.; Riet-Correa, F.; Rodrigues, F.S.; Santos, A.C.; Melo, G.K.A.; Silva, J.A.; Ferreira, R.; Itavo, C.C.B.F.; Lemos, R.A.A. Poisoning by Brachiaria brizantha in flocks of naïve and experienced sheep. Toxicon 2014, 82, 1–8, doi:10.1016/j.toxicon.2014.02.008.
  • Flåøyen, A. A difference in susceptibility of two breeds of sheep to the ’alveld toxin’. Vet. Res. Commun. 1991, 15, 455–457, doi:10.1007/BF00346543.
  • Ferrer, L.M.; Ortín, A.; Loste, A.; Fernández, A.; Verde, M.T.; Ramos, J.J. Photosensitisation in sheep grazing alfalfa infested with aphids and ladybirds. Vet. Rec. 2007, 161, 312–313, doi:10.1136/vr.161.9.312.
  • García Barrachina, M.; González Arto, M.; Miguel Ferrer, L. Intoxication with Hypericum perforatum. Study of drowsiness and photosensitivity in sheep. Albéitar 2007, 30–32.
  • Giaretta, P.R.; Panziera, W.; Hammerschmitt, M.E.; Bianchi, R.M.; Galiza, G.J.; Wiethan, I.S.; Bazzi, T.; Barros, C.S. Clinical and pathological aspects of chronic Senecio spp. poisoning in sheep. Pesq. Vet. Bras. 2014, 34, 967–973, doi:10.1590/S0100-736X2014001000008.
  • Glastonbury, J.R.; Doughty, F.R.; Whitaker, S.J.; Sergeant, E. A syndrome of hepatogenous photosensitisation, resembling geeldikkop, in sheep grazing Tribulus terrestris. Aust. Vet. J. 1984, 61, 314–316, doi:10.1111/j.1751-0813.1984.tb07135.x.
  • Golder, H.M.; Moss, N.; Rogers, G.; Jackson, B.; Gannon, N.; Wong, P.; Lean, I.J. Acute photosensitisation and mortality in a herd of dairy cattle in Tasmania. N. Z. Vet. J. 2017, 65, 39–45, doi:10.1080/00480169.2016.1232181.
  • Greenwood, P.E.; Williamson, G.N. An outbreak of facial eczema in sheep. Aust. Vet. J. 1985, 62, 65–66, doi:10.1111/j.1751-0813.1985.tb14241.x.
  • Hansen, D.E.; McCoy, R.D.; Hedstrom, O.R.; Snyder, S.P.; Ballerstedt, P.B. Photosensitization associated with exposure to Pithomyces chartarum in lambs. J. Am. Vet. Med. Assoc. 1994, 204, 1668–1671.
  • İçen, H.; Sekİn, S.; Karataș, A.; Çakmak, F.; Vural, M.E. Hypericum perforatum toxication in Awassi sheep. Yüzüncü yıl Üniversitesi Veteriner Fakültesi Dergisi 2012, 23, 51–53.
  • Kako, M.D.N.; Al-Sultan, I.I.; Saleem, A.N. Studies of sheep experimentally poisoned with Hypericum perforatum. Vet. Hum. Toxicol. 1993, 35, 298–300.
  • Kessell, A.E.; Ladmore, G.E.; Quinn, J.C. An outbreak of primary photosensitisation in lambs secondary to consumption of Biserrula pelecinus (biserrula). Aust. Vet. J. 2015, 93, 174–178, doi:10.1111/avj.12318.
  • Kümper, H. Hypericum perforatum poisoning in sheep. In Tagung der Fachgruppe “Krankheiten der kleinen Wiederkauer”, Giessen, 10. Juni 1988, Giessen, German Federal Republic; Deutsche Veterinärmedizinische Gesellschaft: Giessen, German Federal Republic, 1988; pp 86–89.
  • Lancaster, M.J.; Vit, I.; Lyford, R.L. Analysis of bile crystals from sheep grazing Panicum schinzii (sweet grass). Aust. Vet. J. 1991, 68, 281, doi:10.1111/j.1751-0813.1991.tb03246.x.
  • Marasas, W.F.; Adelaar, T.F.; Kellerman, T.S.; Minné, J.A.; van Rensburg, I.B.; Burroughs, G.W. First report of facial eczema in sheep in South Africa. Onderstepoort J. Vet. Res. 1972, 39, 107–112.
  • Micheloud, J.F.; Colque-Caro, L.A.; Comini, L.R.; Cabrera, J.L.; Núñez-Montoya, S.; Martinez, O.G.; Gimeno, E.J. Spontaneous photosensitization by Heterophyllaea pustulata Hook. f. (Rubiaceae), in sheep from Northwestern Argentina. Trop Anim Health Prod 2017, 49, 1553–1556, doi:10.1007/s11250-017-1354-0.
  • Naci; HAYDARDEDEOĞLU, O. Hepatogenous photosensitization in Akkaraman lambs: special emphasis to oxidative stress and thrombocytopenia. Veteriner Fakültesi dergisi 2013, 60, 116–122, doi:10.1501/Vetfak_0000002564.
  • Nazifi, S.; Ghane, M.; Fazeli, M.; Ghafari, N.; Azizi, S.; Mansourian, M. Proso millet (Panicum miliaceum) poisoning in Iranian fat-tailed sheep. Comp Clin Pathol 2009, 18, 249–253, doi:10.1007/s00580-008-0784-5.
  • Oertli, E.H.; Rowe, L.D.; Lovering, S.L.; Ivie, G.W.; Bailey, E.M. Phototoxic effect of Thamnosma texana (Dutchman’s breeches) in sheep. American Journal of Veterinary Research 1983, 44, 1126–1129.
  • Ozmen, O.; Sahinduran, S.; Haligur, M.; Albay, M.K. Clinicopathological studies on facial eczema outbreak in sheep in Southwest Turkey. Trop Anim Health Prod 2008, 40, 545–551, doi:10.1007/s11250-008-9132-7.
  • Petazzi, F.; Rubino, G.; Pieragostini, E.; Giordano, G. Photosensitization caused by Hypericum species. Changes in the blood proteins of Ionica goats. Summa 2002, 19, 25–27.
  • Peterson, J.E.; Payne, A.; Culvenor, C.C. Heliotropium europaeum poisoning of sheep with low liver copper concentrations and the preventive efficacy of cobalt and antimethanogen. Aust. Vet. J. 1992, 69, 51–56, doi:10.1111/j.1751-0813.1992.tb07448.x.
  • Puoli, J.R.; Reid, R.L.; Belesky, D.P. Photosensitization in Lambs Grazing Switchgrass. Agronomy Journal 1992, 84, 1077–1080, doi:10.2134/agronj1992.00021962008400060033x.
  • Quinn, J.C.; Chen, Y.; Hackney, B.; Tufail, M.S.; Weston, L.A.; Loukopoulos, P. Acute-onset high-morbidity primary photosensitisation in sheep associated with consumption of the Casbah and Mauro cultivars of the pasture legume Biserrula. BMC veterinary research 2018, 14, 11, doi:10.1186/s12917-017-1318-7.
  • Regnault, T.R. Secondary photosensitisation of sheep grazing bambatsi grass (Panicum coloratum var makarikariense). Aust. Vet. J. 1990, 67, 419, doi:10.1111/j.1751-0813.1990.tb03040.x.
  • Riet-Correa, F.; Haraguchi, M.; Dantas, A.F.M.; Burakovas, R.G.; Yokosuka, A.; Mimaki, Y.; Medeiros, R.M.; Matos, P.F. de. Sheep poisoning by Panicum dichotomiflorum in northeastern Brazil. Pesq. Vet. Bras. 2009, 29, 94–98, doi:10.1590/S0100-736X2009000100015.
  • Saturnino, K.C.; Mariani, T.M.; Barbosa-Ferreira, M.; Brum, K.B.; Fernandes, C.E.d.S.; Lemos, R.A. Intoxicação experimental por Brachiaria decumbens em ovinos confinados. Pesq. Vet. Bras. 2010, 30, 195–202, doi:10.1590/S0100-736X2010000300002.
  • Sinclair, D.P. Pithomyces chartarum spores on pasture and their relation to facial eczema in sheep. New Zealand Journal of Agricultural Research 1961, 4, 492–503, doi:10.1080/00288233.1961.10431607.
  • Stafford, K.J.; West, D.M.; Alley, M.R.; Waghorn, G.C. Suspected photosensitisation in lambs grazing birdsfoot trefoil (Lotus corniculatus). N. Z. Vet. J. 1995, 43, 114–117, doi:10.1080/00480169.1995.35866.
  • Stroebel, J.C. Induction of photosensitivity in sheep with Erodium moschatum (L.) L’Hérit. J. S. Afr. Vet. Assoc. 2002, 73, 57–61, doi:10.4102/jsava.v73i2.556.
  • Wisløff, H.; Wilkins, A.L.; Scheie, E.; Flåøyen, A. Accumulation of sapogenin conjugates and histological changes in the liver and kidneys of lambs suffering from alveld, a hepatogenous photosensitization disease of sheep grazing Narthecium ossifragum. Vet. Res. Commun. 2002, 26, 381–396, doi:10.1023/a:1016298929610.
5.
Other animals
  • Birgel Junior, E.H.; dos Santos, M.C.; Ramos, J.A.C. de; Pogliani, F.C.; Birgel, D.B.; Della Libera, A.M.M.P.; Gregory, L.; Araujo, W.P. de; Benesi, F.J. Secondary hepatogenous photosensitization in a llama (Lama glama) bred in the state of Sáo Paulo, Brazil. Can. Vet. J. 2007, 48, 323–324, doi:10.4141/cjas68-044.
  • Byrne, K.V. Dermatitis in White Pigs Due to Photosensitization. Aust. Vet. J. 1937, 13, 74–75, doi:10.1111/j.1751-0813.1937.tb01152.x.
  • Griffiths, I.B.; Douglas, R.G. Phytophotodermatitis in pigs exposed to parsley (Petroselinum crispum). Vet. Rec. 2000, 146, 73–74, doi:10.1136/vr.146.3.73.
  • Johnson, J.H.; Jensen, J.M. Hepatotoxicity and Secondary Photosensitization in a Red Kangaroo (Megaleia rufus) Due to Ingestion of Lantana camara. Journal of Zoo and Wildlife Medicine 1998, 29, 203–207.
  • Oliveira, C.H.S. de; Barbosa, J.D.; Oliveira, C.M.C.; Bastianetto, E.; Melo, M.M.; Haraguchi, M.; Freitas, L.G.L.; Silva, M.X.; Leite, R.C. Hepatic photosensitization in buffaloes intoxicated by Brachiaria decumbens in Minas Gerais state, Brazil. Toxicon 2013, 73, 121–129, doi:10.1016/j.toxicon.2013.07.001.
  • Smith, B.L.; Asher, G.W.; Thompson, K.G.; Hoggard, G.K. Hepatogenous photosensitisation in fallow deer (Dama dama) in New Zealand. N. Z. Vet. J. 1997, 45, 88–92, doi:10.1080/00480169.1997.36001.
  • Steventon, C.A.; Raidal, S.R.; Quinn, J.C.; Peters, A. Steroidal Saponin Toxicity In Eastern Grey Kangaroos (Macropus Giganteus): A Novel Clinicopathologic Presentation Of Hepatogenous Photosensitization. J. Wildl. Dis. 2018, 54, 491–502, doi:10.7589/2017-03-066.
  • Woolford, L.; Fletcher, M.T.; Boardman, W.S.J. Suspected pyrrolizidine alkaloid hepatotoxicosis in wild southern hairy-nosed wombats (Lasiorhinus latifrons). J. Agric. Food Chem. 2014, 62, 7413–7418, doi:10.1021/jf405811n.
6.
Goat + sheep
  • Opasina, B.A. Photosensitization jaundice syndrome in West African dwarf sheep and goats grazed on Brachiaria decumbens. Tropical Grasslands 1985, 19, 120–123.
  • Jacob, R.H.; Peet, R.L. Poisoning of sheep and goats by Tribulis terrestris (caltrop). Aust. Vet. J. 1987, 64, 288–289, doi:10.1111/j.1751-0813.1987.tb15966.x.
  • Cattle + Sheep
  • van Halderen, A.; Harding, W.R.; Wessels, J.C.; Schneider, D.J.; Heine, E.W.; van der Merwe, J.; Fourie, J.M. Cyanobacterial (blue-green algae) poisoning of livestock in the western Cape Province of South Africa. J. S. Afr. Vet. Assoc. 1995, 66, 260–264.
  • Dollahite, J.W.; Younger, R.L.; Hoffman, G.O. Photosensitization in cattle and sheep caused by feeding Ammi majus (Greater Ammi; bishop’s weed). American Journal of Veterinary Research 1978, 39, 193–197.
7.
Horse + other animals
  • Knupp, S.N.R.; Borburema, C.C.; Oliveira Neto, T.S.; Medeiros, R. de; Knupp, L.S.; Riet-Correa, F.; Lucena, R.B. Surtos de fotossensibilização primária em equídeos causados por Froelichia humboldtiana. Pesq. Vet. Bras. 2014, 34, 1191–1195, doi:10.1590/S0100-736X2014001200008.
8.
Sheep + horse
  • Pimentel, L.A.; Riet-Correa, F.; Guedes, K.M.; Macêdo, J.T.; Medeiros, R.M.; Dantas, A.F. Fotossensibilização primária em eqüídeos e ruminantes no semi-árido causada por Froelichia humboldtiana (Amaranthaceae). Pesq. Vet. Bras. 2007, 27, 23–28, doi:10.1590/S0100-736X2007000100005.
9.
Goat + Sheep + Cattle
  • Bale, S. Poisoning of sheep, goats and cows by the weed Hypericum triquetrifolium. Refuah Veterinarith 1978, 35, 36–37.
10.
Goat + Horse
  • Stegelmeier, B.L.; Colegate, S.M.; Knoppel, E.L.; Rood K. A.; Collert, M.G. Wild parsnip (Pastinaca sativa)-induced photosensitization. Toxicon 2019, 167, 60–66, doi:10.1016/j.toxicon.2019.06.007.
11.
Cattle + Sheep + Horse
  • Mendonça, M.F.F.; Pimentel, L.A.; Leal, P.V.; Oliveira Filho, J.C.; Caymmi, L.G.; Silva, A.W.O.; Jesus, R.S.; Peixoto, T.C. Hepatogenous photosensitization in ruminants and horses caused by the ingestion of Chamaecrista serpens in Brazil. Toxicon 2021, 193, 13–20, doi:10.1016/j.toxicon.2021.01.013.

References

  1. Gupta, R.C. Veterinary Toxicology; Elsevier: Amsterdam, The Netherlands, 2007. [Google Scholar]
  2. Plumlee, K.H. Veterinary Toxicology; Mosby (Elsevier): Amsterdam, The Netherlands, 2004; Volume 1, p. 477. [Google Scholar]
  3. Aboling, S.; Scharmann, F.; Bunzel, D. Equine atypical myopathy: Selection of sycamore maple seedlings (Acer pseudoplatanus L.) in pasture horses is driven by seedling maturity and might be associated with phenolic compounds. Vet. Rec. 2020, 187, e116. [Google Scholar] [CrossRef] [PubMed]
  4. Aboling, S.; Rottmann, S.; Wolf, P.; Jahn-Falk, D.; Kamphues1, J. Case Report: Complex Plant Poisoning in Heavily Pregnant Heifers in Germany. J. Vet. Sci. Technol. 2014, 5, 178. [Google Scholar] [CrossRef]
  5. Petit, R.; Izambart, J.; Guillou, M.; da Silva Almeida, J.R.G.; de Oliveira Junior, R.G.; Sol, V.; Ouk, T.-S.; Grougnet, R.; Quintans-Júnior, L.J.; Sitarek, P.; et al. A Review of Phototoxic Plants, Their Phototoxic Metabolites, and Possible Developments as Photosensitizers. Chem. Biodivers. 2024, 21, e202300494. [Google Scholar] [CrossRef] [PubMed]
  6. Hansen, D.E.; McCoy, R.D.; Hedstrom, O.R.; Snyder, S.P.; Ballerstedt, P.B. Photosensitization associated with exposure to Pithomyces chartarum in lambs. J. Am. Vet. Med. Assoc. 1994, 204, 1668–1671. [Google Scholar] [CrossRef] [PubMed]
  7. Clare, N.T. Photosensitization in Diseases of Domestic Animals: A Review; Commonwealth Agricultural Bureaux: Wallingford, UK, 1952. [Google Scholar]
  8. Collett, M.G. Photosensitisation diseases of animals: Classification and a weight of evidence approach to primary causes. Toxicon X 2019, 3, 100012. [Google Scholar] [CrossRef] [PubMed]
  9. Sinclair, D.P. Pithomyces chartarum spores on pasture and their relation to facial eczema in sheep. N. Z. J. Agric. Res. 1961, 4, 492–503. [Google Scholar] [CrossRef]
  10. Kümper, H. Hypericum perforatum poisoning in sheep. In Tagung der Fachgruppe “Krankheiten der kleinen Wiederkauer”, Giessen, 10 Juni 1988; Deutsche Veterinärmedizinische Gesellschaft: Giessen, Germany, 1988; pp. 86–89. [Google Scholar]
  11. Chen, Y.; Quinn, J.C.; Weston, L.A.; Loukopoulos, P. The aetiology, prevalence and morbidity of outbreaks of photosensitisation in livestock: A review. PLoS ONE 2019, 14, e0211625. [Google Scholar] [CrossRef] [PubMed]
  12. Bornman, J.F.; Barnes, P.W.; Robson, P.R.H.; Robbins, S.A.; Jansen, M.A.K.; Carlos, L. Linkages between stratopheric ozone, UV radiation and climate change and their implications for terrestrial ecosystems. Phytochem. Photobiol. Sci. 2019, 18, 681–716. [Google Scholar] [CrossRef] [PubMed]
  13. Aboling, S. Do Poisonous Plants in Pastures Communicate Their Toxicity?—Metastudy and Evaluation of Pasture Poisoning Cases in Central Europe. Animals 2023, 13, 3795. [Google Scholar] [CrossRef]
  14. Thukral, A.K. A review on measurement of Alpha diversity in biology. Agric. Res. J. 2017, 54, 1–10. [Google Scholar] [CrossRef]
  15. Forbes, J.M. Voluntary Food Intake and Diet Selection in Farm Animals, 2nd ed.; CABI: King’s Lynn, UK, 2007. [Google Scholar]
  16. Cuchillo-Hilario, M.; Wrage-Mönnig, N.; Isselstein, J. Forage selectivity by cattle and sheep co-grazing swards differing in plant species diversity. Grass Forage Sci. 2018, 73, 10. [Google Scholar] [CrossRef]
  17. Pfister, J.A.; Cheney, C.D.; Provenza, F.D. Behavioral toxicology of livestock inngesting plant toxins. J. Range Manag. 1992, 45, 30–36. [Google Scholar] [CrossRef]
  18. Miller, S.M.; Thompson, R.P. Seasonal patterns of diet composition, herbage intake and digestibility limit the performance of cattle grazing native pasture in the Falkland Islands. Grass Forage Sci. 2007, 62, 135–144. [Google Scholar] [CrossRef]
  19. Provenza, F.D.; Villalba, J.J.; Bryant, J.P. Foraging by herbivores: Linking the biochemical diversity of plants to herbivore culture and landscape diversity. In Landscape Ecology and Resource Management. Linking Theory with Practice; Bissonette, J.A., Storch, I., Eds.; Island Press: Washington, DC, USA, 2003; pp. 387–421. [Google Scholar]
  20. Smith, B.L.; Asher, G.W.; Thompson, K.G.; Hoggard, G.K. Hepatogenous photosensitisation in fallow deer (Dama dama) in New Zealand. N. Z. Vet. J. 1997, 45, 88–92. [Google Scholar] [CrossRef] [PubMed]
  21. Sargison, N.D.; Baird, G.J.; Sotiraki, S.; Gilleard, J.S.; Busin, V. Hepatogenous photosensitisation in Scottish sheep casued by Dicrocoelium dendriticum. Vet. Parasitol. 2012, 189, 233–237. [Google Scholar] [CrossRef] [PubMed]
  22. Diamantino, G.M.L.; Pierezan, F.; Ferreira, M.I.C.; Rocha, W.S.D.; Veiga, V.M.O.; Martins, C.E.; Veiga, M.O.; Soto-Blanco, B. Photosensitization by Brachiaria ruziziensis in a sheep herd. Toxicon 2020, 185, 1–4. [Google Scholar] [CrossRef] [PubMed]
  23. Johnson, A.E. Toxicologic Aspects of Photosensitization in Livestock. JNCI J. Natl. Cancer Inst. 1982, 69, 253–258. [Google Scholar] [CrossRef] [PubMed]
  24. Giles, C.J. Outbreak of ragwort (Senecio jacobea) poisoning in horses. Equine Vet. J. 1983, 15, 248–250. [Google Scholar] [CrossRef]
  25. Vesonder, R.; Haliburton, J.; Stubblefield, R.; Gilmore, W.; Peterson, S. Aspergillus flavus and aflatoxins B1, B2, and M1 in corn associated with equine death. Arch. Environ. Contam. Toxicol. 1991, 20, 151–153. [Google Scholar] [CrossRef]
  26. Gehlen, H.; May, A.; Venner, M. Lebererkrankungen beim Pferd. Pferdeheilkunde 2010, 26, 668–679. [Google Scholar] [CrossRef]
  27. Smith, B.L.; O’Hara, P.J. Bovine photosensitization in New Zealand. N. Z. Vet. J. 1978, 26, 2–5. [Google Scholar] [CrossRef] [PubMed]
  28. Stickdorn, T.; Ellis, A.D.; Kienzle, E. Horse feed hygiene evaluation with microbial and sensory examination. In Forages and Grazing in Horse Nutrition; Saastamoinen, M., Fradinho, M.J., Santos, A.S., Miraglia, N., Eds.; Wageningen Academic Publisher: Wageningen, The Netherlands, 2012; Volume 132. [Google Scholar]
  29. Ellenberg, H. Indicator Values of Plants in Central Europe (Zeigerwerte von Pflanzen in Mitteleuropa); E. Goltze: Göttingen, Germany, 1991; Volume 18, p. 248. [Google Scholar]
  30. Dierschke, H.; Briemle, G. Kulturgrasland; Ulmer: Stuttgart, Germany, 2002. [Google Scholar]
  31. Cann, A.J. Mathe für Biologen; Wiley VCH-Verlag: Mörlenbach, Germany, 2004. [Google Scholar]
  32. Chorus, I.; Welker, M. Toxic Cyanobacteria in Water: A Guide to Their Public Health Consequences, Monitoring and Management; Taylor & Francis: London, UK, 2021. [Google Scholar]
  33. Piruzyan, L.; Ostrovskii, M.; Landau, M. “ Sensory” safety of drugs: Photosensitized injury to structures of the eye. Biol. Bull. Acad. Sci. USSR 1991, 18, 29. [Google Scholar]
  34. Frohne, D.; Jensen, U. Systematik des Pflanzenreichs unter Besonderer Berücksichtigung Chemischer Merkmale und Pflanzlicher Drogen, 5th ed.; Wissenschaftliche Verlagsgesellschaft: Stuttgart, Germany, 1998; p. 371. [Google Scholar]
  35. Opasina, B.A. Photosensitization jaundice syndrome in West African dwarf sheep and goats grazed on Brachiaria decumbens. Trop. Grassl. 1985, 19, 120–123. [Google Scholar]
  36. Knupp, S.N.R.; Borburema, C.C.; Oliveira Neto, T.S.; Medeiros, R.d.; Knupp, L.S.; Riet-Correa, F.; Lucena, R.B. Surtos de fotossensibilização primária em equídeos causados por Froelichia humboldtiana. Pesqui. Veterinária Bras. 2014, 34, 1191–1195. [Google Scholar] [CrossRef]
  37. Bale, S. Poisoning of sheep, goats and cows by the weed Hypericum triquetrifolium. Refuah Vet. 1978, 35, 36–37. [Google Scholar]
  38. Colon, J.L.; Jackson, C.A.; Del Piero, F. Case Presentation: Hepatic Dysfunction and Photodermatitis Secondary to Alsike Clover Poisoning. Compend. Equine Rounds 1996, 18, 1022–1026. Available online: https://www.cabidigitallibrary.org/doi/full/10.5555/19972202735 (accessed on 27 May 2024).
  39. Chen, Y.; Loukopoulos, P.; Xie, G.; Quinn, J.C. Relative perceptions of prevalence, impact and importance of photosensitisation in Australian livestock: A survey of veterinarians, livestock traders and livestock producers. Aust. Vet. J. 2022, 100, 388–396. [Google Scholar] [CrossRef] [PubMed]
  40. Araya, O.S.; Ford, E.J.H. An investigation of the type of photosensitization caused by the ingestion of St John’s Wort (Hypericum perforatum) by calves. J. Comp. Pathol. 1981, 91, 135–141. [Google Scholar] [CrossRef] [PubMed]
  41. Winter, J.C.; Thieme, K.; Eule, J.C.; Saliu, E.-M.; Kershaw, O.; Gehlen, H. Photodermatitis and ocular changes in nine horses after ingestion of wild parsnip (pastinaca sativa). BMC Vet. Res. 2022, 18, 80. [Google Scholar] [CrossRef]
  42. Puschner, B.; Chen, X.; Read, D.; Affolter, V. Alfalfa hay induced primary photosensitization in horses. Vet. J. 2016, 211, 32–38. [Google Scholar] [CrossRef]
  43. Iason, G.R.; Villalba, J.J. Behavioral Strategies of Mammal Herbivores Against Plant Secondary Metabolites: The Avoidance-Tolerance Continuum. J. Chem. Ecol. 2006, 32, 115–1132. [Google Scholar] [CrossRef] [PubMed]
  44. Leiber, F.; Walkenhorst, M.; Holinger, M. The relevance of feed diversity and choice in nutrition of ruminant livestock. Landbauforschung 2020, 70, 35. [Google Scholar] [CrossRef]
  45. Opitz von Boberfeld, W. Grünlandlehre; UTB: Stuttgart, Germany, 1994. [Google Scholar]
  46. Provenza, F.D.; Pfister, J.A.; Cheney, C.D. Mechanisms of learning in diet selection with reference to phytotoxicosis in herbivores. J. Range Manag. 1992, 45, 36–45. [Google Scholar] [CrossRef]
  47. Crawley, M.J.; Johnston, A.E.; Silvertown, J.; Dodd, M.; Mazancourt, C.D.; Heard, M.S.; Henman, D.F.; Edwards, G.R. Determinants of Species Richness in the Park Grass Experiment. Am. Nat. 2005, 165, 179–192. [Google Scholar] [CrossRef] [PubMed]
  48. Oruc, H.H.; Akkoc, A.; Uzunoglu, I.; Kennerman, E. Nitrate Poisoning in Horses Associated With Ingestion of Forage and Alfalfa. J. Equine Vet. Sci. 2010, 30, 159–162. [Google Scholar] [CrossRef]
  49. Vondran, S.E.A. Effects of alfalfa chaff on the gastric mucosa in adult horses. Pferdeheilkunde 2017, 33, 66–71. [Google Scholar] [CrossRef]
  50. Chizzola, R.; Tollemache, D.O. Skin lesions of horses- provoked by poisonous plants? Wien. Tieraerztliche Monatsschrift 1992, 79, 120–121. [Google Scholar]
  51. Calapai, G.; Miroddi, M.; Minciullo, P.L.; Caputi, A.P.; Gangemi, S.; Schmidt, R.J. Contact dermatitis as an adverse reaction to some topically used European herbal medicinal products—Part 1: Achillea millefolium-Curcuma longa. Contact Dermat. 2014, 71, 1–12. [Google Scholar] [CrossRef] [PubMed]
  52. Vogt-Andersen, U.; Calov, B. Long-term effects of sheep grazing on giant hogweed (Heracleum mantegazzianum). Hydrobiologia 1996, 340, 277–284. [Google Scholar] [CrossRef]
  53. Rosa García, R.; Celaya, R.; García, U.; Osoro, K. Goat grazing, its interactions with other herbivores and biodiversity conservation issues. Small Rumin. Res. 2012, 107, 49–64. [Google Scholar] [CrossRef]
Agriculture 14 01137 g001
Figure 1. Key variables, principal variables, and subvariables used for data analysis.
Figure 1. Key variables, principal variables, and subvariables used for data analysis.
Agriculture 14 01137 g001
Agriculture 14 01137 g002
Figure 2. Key and principal variables and the most important subvariables, marked in red.
Figure 2. Key and principal variables and the most important subvariables, marked in red.
Agriculture 14 01137 g002
Agriculture 14 01137 g003
Figure 3. Composition of the data material. “Proven” means that the author proved the identity of the phototoxic organism. “Suspected” means that the author suspected the identity of the phototoxic organism. “Verified” means that the author’s indication of the phototoxic potential of the respective organism was checked in the present study by a second source.
Figure 3. Composition of the data material. “Proven” means that the author proved the identity of the phototoxic organism. “Suspected” means that the author suspected the identity of the phototoxic organism. “Verified” means that the author’s indication of the phototoxic potential of the respective organism was checked in the present study by a second source.
Agriculture 14 01137 g003
Agriculture 14 01137 g004
Figure 4. Case reports (n) differentiated according to the phototoxic organisms. Yellow: verified cases. Red: non-verified cases. Ntotal = 172.
Figure 4. Case reports (n) differentiated according to the phototoxic organisms. Yellow: verified cases. Red: non-verified cases. Ntotal = 172.
Agriculture 14 01137 g004
Table 1. Case reports (n) and their origin, and level of feed examination.
Table 1. Case reports (n) and their origin, and level of feed examination.
ContinentCases (n) Portion (%)Feed Examination by Authors
CompletelyPartlyUnknown
South America5431.4311310
Australia3822.114204
North America3319.218105
Europe148.1293
Asia127.0354
New Zealand116.4344
Africa84.7161
India21.2002
Sum (n)172-726733
Portion (%)-10041.939.019.2
Table 2. Effect of different feed qualities on incidence of photosensitization in different animal species.
Table 2. Effect of different feed qualities on incidence of photosensitization in different animal species.
Animal SpeciesNormal Feed QualityPoor Feed QualityTotal
Sheep60969
Cattle451055
Horse30131
Goat11011
Other animals 210111
Sum (n)15621177 1
Portion (%)88.111.9100
1 The authors of four publications ([35,36,37,38]; described cases in which more than one animal species was involved, resulting in slightly higher number of animals (n = 177) than case reports (n = 172). 2 Identifications in the category “other animals” consisted of nine species, four domestic ones (pig, donkey, water buffalo, and buffalo) and five wild ones (fallow deer, gray and red kangaroo, hairy-nosed wombat, and llama).
Table 3. Incidence of distinct kinds of photosensitization in different animal species.
Table 3. Incidence of distinct kinds of photosensitization in different animal species.
Animal
Species		Primary PhotosensitizationSecondary PhotosensitizationUnknown Kind of PhotosensitizationTotal
Sheep2244369
Cattle13291355
Horse1810331
Goat47011
Other animals28111
Sum (n)599820177
Portion (%)33.355.411.3100
Table 4. Effect of different kinds of feed on incidence of photosensitization in different animal species.
Table 4. Effect of different kinds of feed on incidence of photosensitization in different animal species.
Animal SpeciesKind of FeedSum (n)
FreshConservedBothUnknown
Sheep5943369
Cattle3975455
Horse13133231
Goat900211
Other animals713011
Sum (n)127251411177
Portion (%)71.814.17.96.2100
Table 5. Effect of plant diversity and feed choice on incidence of photosensitization per kind of feed.
Table 5. Effect of plant diversity and feed choice on incidence of photosensitization per kind of feed.
FeedstuffHigh
Diversity		Low
Diversity		Unknown Level
of Diversity		Sum of Animals (n)Feed ChoiceNo Feed ChoiceUnknown Possibility of Feed ChoiceSum of Animals (n)
Fresh feed21565012788336127
Conserved feed512825322025
Fresh and conserved feed6531446414
Unknown feed condition0471102911
Sum (n)3277681771511349177
(%)18.143.538.41008.563.827.7100
Table 6. Effect of feed diversity and choice on incidence of photosensitization in different animal species.
Table 6. Effect of feed diversity and choice on incidence of photosensitization in different animal species.
Animal SpeciesHigh
Diversity		Low
Diversity		Unknown Level of DiversitySumFeed ChoiceNo feed ChoiceUnknown Possibility of Feed ChoiceSum
Sheep83526698431869
Cattle122122554361555
Horse8121131221831
Goat2451108311
Other animals2541115511
Sum (n)3277681771511349177
Portion (%)18.143.538.41008.563.827.7100
Disclaimer/Publisher’s Note: The statements, opinions and data contained in all publications are solely those of the individual author(s) and contributor(s) and not of MDPI and/or the editor(s). MDPI and/or the editor(s) disclaim responsibility for any injury to people or property resulting from any ideas, methods, instructions or products referred to in the content.

Share and Cite

MDPI and ACS Style

Moritz, R.; Aboling, S. Incidence of Photosensitization in Husbandry Animals: A Meta-Study on the Effects of Feed Diversity and Feed Choice. Agriculture 2024, 14, 1137. https://doi.org/10.3390/agriculture14071137

AMA Style

Moritz R, Aboling S. Incidence of Photosensitization in Husbandry Animals: A Meta-Study on the Effects of Feed Diversity and Feed Choice. Agriculture. 2024; 14(7):1137. https://doi.org/10.3390/agriculture14071137

Chicago/Turabian Style

Moritz, Rieke, and Sabine Aboling. 2024. "Incidence of Photosensitization in Husbandry Animals: A Meta-Study on the Effects of Feed Diversity and Feed Choice" Agriculture 14, no. 7: 1137. https://doi.org/10.3390/agriculture14071137

Note that from the first issue of 2016, this journal uses article numbers instead of page numbers. See further details here.

Article Metrics

Back to TopTop