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  • Systematic Review
  • Open Access

21 February 2025

Molecular Prevalence of Avian Haemosporidian Parasites in Southeast Asia: Systematic Review and Meta-Analysis

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1
Faculty of Veterinary Medicine, Western University, Kanchanaburi 71170, Thailand
2
Department of Animals Science, Faculty of Natural Resources, Rajamangala University of Technology Isan, Sakon Nakhon 47160, Thailand
3
Department of Veterinary Medicine, Facultry of Agriculture, National University of Laos, Vientiane 7322, Laos
4
Department of Infectious Diseases and Public Health, Jockey Club College of Veterinary Medicine and Life Sciences, City University of Hong Kong, Hong Kong SAR, China
Animals2025, 15(5), 636;https://doi.org/10.3390/ani15050636
This article belongs to the Special Issue Wild and Domestic Animal Hemoparasites
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Simple Summary

This systematic review reveals that the prevalences of Plasmodium, Haemoproteus and Leucocytozoon in Southeast Asia are 21% (95% CI: 18–25%), 18% (95% CI: 15–22%) and 34% (95% CI: 30–37%), respectively. Additionally, this review reveals 23 lineages of Plasmodium, 35 lineages of Haemoproteus and 21 lineages of Leucocytozoon identified in avian species throughout Southeast Asia. These findings indicate that monitoring of these parasites in domestic poultry and wild birds should be implemented. Furthermore, the high genetic diversity suggests the existence of undescribed species. Thus, further experimental studies applying combined microscopic and molecular techniques may reveal overlooked parasites.

Abstract

In this study, for the first time, a systematic review and meta-analysis were conducted to understand the prevalence and genetic diversity of haemosporidian parasites—namely, Plasmodium, Haemoproteus and Leucocytozoon—in avian species in Southeast Asia. Following the PRISMA guidelines, 14,211 studies were retrieved from PubMed, ScienceDirect and Scopus, which contain data relevant to ‘Plasmodium’ or ‘Haemoproteus’ or ‘Leucocytozoon’ and ‘birds’ or ‘chickens’. Of these, 15 articles reporting the prevalence of Plasmodium, Haemoproteus or Leucocytozoon in Southeast Asia were selected for meta-analysis. The pooled prevalence estimates with 95% confidence intervals (CIs) of Plasmodium, Haemoproteus and Leucocytozoon were analyzed using a meta-analysis of their proportions, implemented in R programming. The publication bias was checked using a funnel plot and Egger’s test. Consequently, the pooled prevalences of Plasmodium, Haemoproteus and Leucocytozoon in Southeast Asia were found to be 21% (95% CI: 18–25%), 18% (95% CI: 15–22%) and 34% (95% CI: 30–37%), respectively. The prevalence of Plasmodium in domestic poultry (37.94%) was found significantly higher than in wild birds (6.46%). There was substantial heterogeneity among studies related to Plasmodium (χ2 = 171.50, p < 0.0001, I2 = 94.84%), Haemoproteus (χ2 = 52.20, p < 0.0001, I2 = 90.4%) and Leucocytozoon (χ2 = 433.90, p < 0.0001, I2 = 98.80%). Additionally, this review revealed 23 lineages of Plasmodium, 35 lineages of Haemoproteus and 21 lineages of Leucocytozoon reported from both domestic poultry and wild birds in Southeast Asia. In conclusion, this systematic review suggested that the prevalence of avian haemosporidian parasites in Southeast Asia is high. Particularly, domestic poultry has a high prevalence of Plasmodium, suggesting that monitoring of this parasite should be implemented in the poultry production system. Furthermore, several parasites found in wild birds are undescribed species. Further experimental studies using combined microscopic and molecular techniques might reveal the characteristics of overlooked parasites.

1. Introduction

Haemosporidian parasites are a group of vector-borne parasites belonging to the order Haemosporida, which are classified into four families: Haemoproteidae (Haemoproteus), Plasmodiidae (Plasmodium), Leucocytozoidae (Leucocytozoon) and Garniidae (Fallisia) [1,2]. During the first half of the 20th century, the term ‘malaria parasites’ was used broadly for all haemosporidian parasites, but later, the term was dropped because of the differences in basic biological characteristics among these parasites [3]. More recently, the term ‘malaria parasites’ has been restricted to the haemosporidian parasites belonging to the genus Plasmodium. Diseases caused by Plasmodium, Haemoproteus and Leucocytozoon are named malaria, haemoproteosis and leucocytozoonosis, respectively [3]. The vectors of these parasites are as follows: Culex, Aedes and Culiseta mosquitoes for Plasmodium, biting midges and hippoboscids for Haemoproteus, and simuliids for Leucocytozoon [1]. However, one species of Leucocytozoon (Leucocytozoon caulleryi) can also be transmitted by biting midges.
Recently, 55 morphospecies of Plasmodium, 177 morphospecies of Haemoproteus and 45 morphospecies of Leucocytozoon have been described in birds [4,5,6]. Furthermore, PCR-based techniques [7,8] amplifying the fragment cytochrome b gene of these parasites showed huge genetic diversity, comprising ~5131 described lineages deposited in a haemosporidian-specific public database (the MalAvi database, accessed on November 2024) [9]. Some of haemosporidian parasites, such as Plasmodium elongatum [10], Plasmodium gallinaceum [11], Plasmodium homocircumflexum [12], Plasmodium relictum [13], Haemoproteus minitus [14] and L. caulleryi [15], can cause severe diseases in non-adapted hosts. Generally, Plasmodium can rupture the red blood cells of birds, resulting in anemia, weakness and eventually death [16]. Additionally, the development of the exo-erythrocytic stage in the brain can cause cerebral capillary blockage, resulting in ischemia [17,18]. Furthermore, infected birds can die because of hypoxemia, secondary to the severe pulmonary pathology [19]. Haemoproteus infection may lead to the damage of internal organs caused by the development of the exo-erythrocytic megalomeront stage [14]. Megalomeronts of Haemoproteus might also induce myositis in an infected host [20]. In the case of Leucocytozoon, the parasite can cause lethal hemorrhagic disease [21], anemia, anorexia, lethargy, green dropping and decreased egg production [1].
The prevalence and transmission of haemosporidian parasites among birds were reported in Southeast Asia [22], suggesting concerns in poultry production and wild bird conservation. Previously, a systematic review and meta-analysis of the global prevalence of Plasmodium infection in wild birds was published [16]. However, this study only included avian Plasmodium in Indonesia [23], thus lacking information from other countries in Southeast Asia. To fill the gap, a systematic review and meta-analysis were performed in this study to estimate the molecular prevalence of avian Plasmodium and other haemosporidian parasites in Southeast Asia, considering geographical locations, avian host species and their heterogeneity. This study provides novel information about the prevalence of Plasmodium, Haemoproteus and Leucocytozoon in Southeast Asia. Furthermore, this review reveals the genetic diversity of Plasmodium and other haemosporidian parasites, providing baseline information for future experimental studies and the development of preventive measures.

2. Materials and Methods

2.1. Study Protocol, Literature Search and Screening

The systematic review and meta-analysis was conducted following the PRISMA guidelines [24]. The review protocol has been registered in the Open Science Framework (https://doi.org/10.17605/OSF.IO/ZS9UW). All published articles that reported the prevalence of avian haemosporidians (Plasmodium, Haemoproteus and Leucocytozoon) were retrieved from three bibliographic databases, namely PubMed, ScienceDirect and Scopus. The search string was used as follows: (“Plasmodium” OR “Leucocytozoon” OR “Haemoproteus” OR “blood parasites”) AND (“bird” OR “chicken”). The papers published until 31 October 2024 were included. Title and abstract screening were performed independently by three reviewers (K.S., N.SR. and N.SO.).

2.2. Article Selection and Quality Assessment

Papers were selected for the systematic review if they met the predefined inclusion criteria. The inclusion criteria were as follows: (i) study performed in any avian species; (ii) cross-sectional study; (iii) locations within Southeast Asia; (iv) sample size of greater than 25; (v) study that used PCR-based detection method; and (vi) exact total and positive number (or prevalence with 95% confidence interval) were provided. Studies that reported Plasmodium sp., Haemoproteus sp. or Leucocytozoon sp. in non-avian species, case reports, and review articles were excluded.
The quality of selected studies was evaluated using the Quality Assessment Scale applied from the previously published report [25]. Studies were grouped into two groups: low (0–8 scores) and high quality (9–14 scores). The full-text assessment, article selection and quality assessment were independently performed by two reviewers (P.P. and C.J.S.). Disputes were resolved by discussion.

2.3. Data Extraction

Two reviewers (P.P. and T.M.) investigated the included papers thoroughly for data extraction. The extracted data included (i) study characteristics: the authors and year of publication; (ii) study methodology: sampling area, period of study, method used for parasites detection, sample size and number of positive samples; (iii) species and order of birds; and (iv) parasite species.

2.4. Statistical Analysis

Quantitative variables (number of total birds and number of birds infected with Plasmodium spp., Leucocytozoon spp. and Haemoproteus spp.) were pooled and analyzed. The available prevalence data of each parasite with a minimum of three articles were pooled and considered for meta-analysis, which included pooled prevalence of Plasmodium and Leucocytozoon in both wild birds and domestic poultry as well as pooled prevalence of Haemoproteus in wild birds. Meta-analysis of proportion (fixed effect model) was implemented in R (version 4.3.3) [26], following the previously reported guidelines [27]. I2 and Q tests were used to evaluate the heterogeneity among the included studies (p ≥ 0.10 or I2 < 50% indicated low statistical heterogeneity, whereas p ≤ 0.10 or I2 > 50% indicated high statistical heterogeneity) [28]. The results of meta-analysis were visualized by using forest plots. Meta-regression was used to identify any significant differences in the prevalence of Plasmodium and Haemoproteus between regions (mainland and maritime) and host species (domestic poultry and wild birds). Publication bias was assessed in meta-analysis that contained ≥ 10 studies using funnel plots and Egger’s regression test. The funnel plots and Egger’s regression test were performed in R [26] using ‘meta’ (version 8.0-1) and ‘metafor’ (version 4.6-0) packages.

3. Results

3.1. Characteristics of Included Studies (Table 1)

Initially, a total of 14,211 articles were retrieved from the search databases. After deduplication, 446 articles were removed (Figure 1). Subsequently, 13,741 articles that did not meet the selection criteria were excluded based on the screening of titles and abstracts. Full texts of a total of twenty-four articles were investigated for eligibility and ten articles were excluded for the following reasons: one article did not focus on the prevalence of avian haemosporidian parasites [29], two articles provided insufficient data [30,31], three articles did not use the molecular detection methods [32,33,34], two articles shared a dataset with other studies [35,36], one article had a sample size lower than 25 [37] and one article was conducted outside of Southeast Asia [38].
Figure 1. Flowchart for study selection.
Table 1. Characteristics of included studies.
Table 1. Characteristics of included studies.
AuthorYearCountryRegionPeriod of StudyPCR-Based
Detection Method		Information of BirdsInformation of ParasitesPositive CasesSample Size
Boonchuay et al. [39]2023ThailandMainland2021–2022HaemF-HaemR2GalliformesP. gallinaceum757
HaemF-HaemR2GalliformesP. juxtanucleare557
HaemF-HaemR2GalliformesPlasmodium sp.2557
HaemFL-HaemR2LGalliformesL. schoutedeni657
HaemFL-HaemR2LGalliformesLeucocytozoon sp.4557
Chatan et al. [40]2024ThailandMainland2022HaemF-HaemR2GalliformesP. gallinaceum436
HaemF-HaemR2GalliformesP. juxtanucleare136
HaemF-HaemR2GalliformesPlasmodium sp.2036
HaemF-HaemR2AnseriformesPlasmodium sp.1280
Dhamayanti et al. [41]2023IndonesiaMaritime2022HaemOF-HaemORGalliformesP. juxtanucleare2160
Ivanova et al. [42]2010MalaysiaMaritime2010HaemF-HaemR2CoraciiformesPlasmodium sp.09
HaemF-HaemR2CoraciiformesHaemoproteus sp.19
HaemF-HaemR2ApodiformesPlasmodium sp.01
HaemF-HaemR2ApodiformesHaemoproteus sp.01
HaemF-HaemR2ColumbiformesPlasmodium sp.03
HaemF-HaemR2ColumbiformesHaemoproteus sp.13
HaemF-HaemR2PasseriformesPlasmodium sp.462
HaemF-HaemR2PasseriformesHaemoproteus sp.1662
HaemF-HaemR2PiciformesPlasmodium sp.04
HaemF-HaemR2PiciformesHaemoproteus sp.14
Khumpim et al. [35]2021ThailandMainland2019–2020LsF2-LsR2GalliformesL. sabrazesi252313
Lertwatcharasarakul
et al. [43]		2021ThailandMainland2012–2019HaemFL-HaemR2LAccipitriformesLecucocytozoon sp.3198
HaemFL-HaemR2LStrigiformesLecucocytozoon sp.5202
Muriel et al. [44] 2021MyanmarMainland2019HaemF-HaemR2PasseriformesPlasmodium sp.3120
HaemF-HaemR2PasseriformesHaemoproteus sp.8120
HaemF-HaemR2PasseriformesHaems/Plas *1120
HaemF-HaemR2PelecaniformesPlasmodium sp.11
HaemF-HaemR2PelecaniformesHaemoproteus sp.01
HaemF-HaemR2CoraciiformesPlasmodium sp.04
HaemF-HaemR2CoraciiformesHaemoproteus sp.24
HaemF-HaemR2CuculiformesPlasmodium sp.01
HaemF-HaemR2CuculiformesHaemoproteus sp.01
HaemF-HaemR2ColumbiformesPlasmodium sp.01
HaemF-HaemR2ColumbiformesHaemoproteus sp.11
Noni and Tan [45]2023MalaysiaMaritime2021AE983-AE985PasseriformesPlasmodium sp.1429
Piratae et al. [46]2021ThailandMainland2020HaemFL-HaemR2LGalliformesL. schoutedeni5250
HaemFL-HaemR2LGalliformesLecucocytozoon sp.45250
Pornpanom et al. [22]2019ThailandMainland2012–2018HaemF-HaemR2StrigiformesPlasmodium sp.15167
HaemF-HaemR2StrigiformesHaemoproteus sp.41167
HaemF-HaemR2StrigiformesHaem/Plas1167
Pornpanom et al. [47]2021ThailandMainland2013–2019HaemF-HaemR2AccipitriformesPlasmodium sp.5198
HaemF-HaemR2AccipitriformesHaemoproteus sp.8198
Prompiram et al. [48]2023ThailandMainland2018–2019HaemF-HaemR2ColumbiformesH. columbae2487
Subaneg et al. [49]2024ThailandMainland2020–2022HaemF-HaemR2AccipitriformesPlasmodium sp.378
HaemF-HaemR2StrigiformesPlasmodium sp.131
Win et al. [50]2020MyanmarMainland2017–2020HaemFL-HaemR2LGalliformesLecucocytozoon sp.81461
HaemF-HaemR2GalliformesHaem/Plas158461
Yuda [23]2019IndonesiaMaritime2009HaemF-HaemR2PelecaniformesPlasmodium sp.33
HaemF-HaemR2PelecaniformesHaemoproteus sp.03
HaemFL-HaemR2LPelecaniformesLecucocytozoon sp.03
HaemF-HaemR2CharadriiformesPlasmodium sp.340
HaemF-HaemR2CharadriiformesHaemoproteus sp.040
HaemFL-HaemR2LCharadriiformesLecucocytozoon sp.140
HaemF-HaemR2ColumbiformesPlasmodium sp.03
HaemF-HaemR2ColumbiformesHaemoproteus sp.03
HaemFL-HaemR2LColumbiformesLecucocytozoon sp.03
HaemF-HaemR2CuculiformesPlasmodium sp.05
HaemF-HaemR2CuculiformesHaemoproteus sp.15
HaemFL-HaemR2LCuculiformesLecucocytozoon sp.05
HaemF-HaemR2CaprimulgiformesPlasmodium sp.011
HaemF-HaemR2CaprimulgiformesHaemoproteus sp.011
HaemFL-HaemR2LCaprimulgiformesLecucocytozoon sp.011
HaemF-HaemR2ApodiformesPlasmodium sp.014
HaemF-HaemR2ApodiformesHaemoproteus sp.014
HaemFL-HaemR2LApodiformesLecucocytozoon sp.014
HaemF-HaemR2CoraciiformesPlasmodium sp.02
HaemF-HaemR2CoraciiformesHaemoproteus sp.02
HaemFL-HaemR2LCoraciiformesLecucocytozoon sp.0
HaemF-HaemR2PasserinformesPlasmodium sp.134
HaemF-HaemR2PasserinformesHaemoproteus sp.134
HaemFL-HaemR2LPasserinformesLecucocytozoon sp.134
HaemF-HaemR2GalliformesPlasmodium sp.010
HaemF-HaemR2GalliformesHaemoproteus sp.010
HaemFL-HaemR2LGalliformesLecucocytozoon sp.010
HaemF-HaemR2AneriformesPlasmodium sp.110
HaemF-HaemR2AneriformesHaemoproteus sp.010
HaemFL-HaemR2LAneriformesLecucocytozoon sp.010
* Haems/Plas = Haemoproteus or Plasmodium.
Fifteen cross-sectional articles were included in the final qualitative and quantitative analysis. All the characteristics of the included articles are shown in Table 1. Among the fourteen included articles, six articles reported haemosporidian parasites in domestic poultry [35,39,40,41,46,50], eight articles reported haemosporidian parasites in wild birds [22,42,43,44,45,47,48,49] and one article reported haemosporidian parasites in both domestic poultry and wild birds [23]. Likewise, Plasmodium sp. was reported in ten articles on both domestic poultry and wild birds [22,23,39,40,41,42,44,45,47,49]. Haemoproteus sp. was reported in six articles on only wild birds [22,23,42,44,47,48]. Leucocytozoon sp. was reported in six articles on both domestic poultry and wild birds [23,35,39,43,46,50].
Out of the fifteen included articles, two were from Indonesia [23,41], Malaysia [42,45], Myanmar [44,50] each, and nine were from Thailand [22,35,39,40,43,46,47,48,49]. The quality assessment showed that all 15 articles were of high quality (Table 2).
Table 2. Quality assessment of included studies applied from Zhou et al. (2022) [25].

3.2. The Crude Prevalence of Haemosporidian Parasites in Southeast Asia

All 15 included articles investigated a total of 2498 birds. Plasmodium spp. were found in 149 birds. With regard to Plasmodium species, Plasmodium gallinaceum was found in seven domestic chickens (Gallus gallus domesticus) and four turkeys (Meleagris gallopavo). Plasmodium juxtanucleare was found in twenty-six domestic chickens and one turkey. Plasmodium sp. was found in 58 domestic poultry and 53 wild birds (Accipitriformes, Charadriiformes, Passeriformes, Palecaniformes and Strigiformes). Haemoproteus spp. were found in 81 wild birds (Accipitriformes, Columbiformes, Coraciiformes, Cuculiformes, Passeriformes, Piciformes and Strigiformes). With regard to Haemoproteus species, Haemoproteus columbae was found in 24 pigeons (Columba liva). Likewise, Leucocytozoon spp. were found in 444 birds. Among Leucocytozoon species, Leucocytozoon sabrazesi was reported in 252 domestic chickens. Leucocytozoon schoutedeni was found in eleven domestic chickens. Leucocytozoon sp. was found in 171 domestic chickens and 10 wild birds (Accipitriformes, Charadriiformes, Passeriformes and Strigiformes).
The highest prevalence of Plasmodium sp. (64.91%) was reported by Boonchuay et al. (2023) [39], while Pornpanom et al. (2021) [47] reported the lowest prevalence at 2.53%. Likewise, the highest prevalence of Haemoproteus sp. was reported to be 27.59% in the study conducted by Prompiram et al. (2019) [48]. The lowest prevalence of Haemoproteus sp. was 1.79% in the study conducted by Yuda (2019) [23]. The prevalence of Leucocytozoon spp. was in the range of 89.47% [39] to 1.52% [23].

3.3. Genetic Diversity of Haemosporidian Parasites in Southeast Asia

In total, nine articles [22,39,40,42,43,44,45,47,48] reported the lineage of haemosporidian parasites following the MalAvi database (Table 3). The pooled data revealed that only one lineage of Plasmodium gallinaceum (GALLUS01) and one lineage of Plasmodium juxtanucleare (GALLUS02) were found in domestic chickens in Southeast Asia. However, there are six other lineages of Plasmodium sp. that were found to infect domestic poultry. In wild birds, 15 lineages were reported from four orders of avian species (Accipitriformes, Passeriformes, Pelecaniformes and Strigiformes).
Table 3. Summary of avian haemosporidian lineages found in Southeast Asia.
In the case of Haemoproteus sp., 35 lineages were isolated and described from wild birds belonging to six orders (Accipitriformes, Coraciiformes, Columbiformes, Passeriformes, Piciformes and Strigiformes). Sixteen lineages of Leucocytozoon sp. were isolated and described from domestic chickens and five lineages were isolated and described from two orders of wild birds (Accipitriformes and Strigiformes). Furthermore, some lineages including ACCBAD01, ORW1 and FANTAIL01 were found in both domestic poultry and wild birds.

3.4. The Pooled Prevalence Estimate of Haemosporidian Parasites in Southeast Asia

The pooled prevalence of Plasmodium sp. in both wild birds and domestic poultry was comparable among ten articles (21.00%, 95% CI: 18.00–25.00%) (Figure 2). The prevalence of Plasmodium sp. between mainland (14.33%, 95% CI: 11.55–17.12%) and maritime (12.18%, 95% CI: 8.28–16.07%) was not significantly different (Table 4). However, the prevalence of Plasmodium sp. among wild birds (4.77%, 95% CI: 4.77–8.17%) was significantly different from domestic poultry (37.94%, 95% CI: 37.97–43.92%).
Figure 2. Pooled prevalence of Plasmodium in wild birds and domestic poultry [22,23,39,40,41,42,44,45,47,49].
Table 4. Pooled prevalence, heterogeneity and meta-regression in Plasmodium, Haemoproteus and Leucocytozoon infection in Southeast Asia.
The prevalence of Haemoproteus sp. was reported in six papers on wild birds only. The pooled prevalence of Haemoproteus sp. was 18.00% (95% CI: 15.00–22.00%) (Figure 3). The prevalence of Haemoproteus sp. in the mainland region (19.89%, 95% CI: 16.23–24.14%) was significantly different from the maritime region (10.99, 95% CI: 6.56–15.43%) (Table 4). The pooled prevalence of Leucocytozoon sp. in both wild birds and domestic poultry was comparable among the six articles (34.00%, 95% CI: 30.00–37.00%) (Figure 4).
Figure 3. Pooled prevalence of Haemoproteus in wild birds [22,23,42,44,47,48].
Figure 4. Pooled prevalence of Leucocytozoon in wild birds and poultry [23,35,39,43,46,50].

3.5. Publication Bias

The funnel plot (Figure 5) showed publication bias, which was confirmed by Egger’s test (the regression coefficient = -0.0813, 95% CI: −0.1420–−0.0205, p = 0.003). The funnel plot analysis and Egger’s test were not performed for the studies on Haemoproteus and Leucocytozoon because the analysis required a minimum of 10 studies.
Figure 5. Funnel plot for prevalence of avian Plasmodium in Southeast Asia.

4. Discussion

This is the first systematic review and meta-analysis conducted to demonstrate the pooled prevalence estimates of Plasmodium, Haemoproteus and Leucocytozoon infection in wild birds and domestic poultry in Southeast Asia. The results showed that the pooled prevalences of Plasmodium, Haemoproteus and Leucocytozoon were 21%, 18% and 34%, respectively. Southeast Asia has mostly hot and humid tropical climatic zones that might be suitable for the existence of both haemosporidian parasites and their vectors. Previously, it was shown that temperatures above 12 °C and 20 °C were suitable for the completion of sporogony development of Plasmodium sp. and Haemoproteus sp., respectively [51,52]. Likewise, temperatures above 22 °C allow the complete sporogony development of Leucocytozoon sp. [53]. Furthermore, other environmental factors such as high rainfall might also promote the abundance of vectors [35]. Additionally, wild birds and domestic poultry raised in open fields are exposed to blood-sucking insects that are known to transmit blood parasites such as Plasmodium sp., Haemoproteus sp. and Leucocytozoon sp. On the other hand, infected birds that are raised in indoor conditions or in open fields might also shed these parasites, resulting in the further spread of parasites. As a partial remedy, recently, swiftlet houses were designed in Indonesia, Malaysia and Thailand that imitated the environment of natural caves [54]. In Thailand, income generated by selling such swiftlet nests was estimated to be USD 66–100 million per year [54]. However, the occurrence of infectious diseases, including blood parasites in swiftlets (Aerodramus germani) might affect the economy as well.
It was observed that the prevalence of Plasmodium was significantly higher in domestic poultry than in wild birds (Table 4). This might be related to the biology of infected birds, such as hunting activity and defensive behaviors (foot stomping, head and wing movement and tail shaking) [22,49,55]. Interestingly, some Plasmodium-infected birds were migratory birds, such as the Cinerous Vulture (Aegypius monachus) and Himalayan Vulture (Gyps himalayansis) [47,49]. Himalayan Vultures normally reside in the Himalayas from Northern Pakistan to Bhutan, Southern and Eastern Tibet and China [56]. During winter, juveniles might migrate to other South Asian countries [56]. Consequently, there were records of Himalayan Vultures in countries, such as Cambodia, Indonesia, Malaysia, Myanmar, Thailand and Singapore [57]. This migratory pattern of infected birds could play a role in introducing Plasmodium sp. in non-adaptive birds from a new environment, which might lead to clinical signs in naïve birds. Furthermore, the East Asia Flyway of migratory birds lies in Southeast Asia, which connects Northern, Eastern Asia and insular Southeast Asia [58]. Thus, there exists a possibility of Plasmodium infection and transmission in several migratory and native birds. Proper implementation of disease monitoring systems is crucial to prevent the spread of the parasite.
A study on Haemoproteus was conducted in only four countries (Indonesia, Malaysia, Myanmar and Thailand) (Table 1). Furthermore, several lineages were reported from non-described species (Table 3). This was evidence of the existence of a number of overlooked parasites. Thus, it is worth conducting further investigation using combined microscopic and molecular techniques to identify the prevalence of Haemoproteus in birds in Southeast Asia. This will reveal the existence of undescribed species, if any. In the case of Leucocytozoon, the prevalence of the parasite was very high in domestic poultry (Table 4). Parasite species that are known for their low pathogenicity such as Leucocytozoon sabrazesi and Leucocytozoon schoutedeni were reported. However, there was a report on the pathology and molecular characteristics of a lethal parasite (Leucocytozoon caulleryi) in Thailand [21]. Although L. sabrazesi and L. schoutedeni might not be pathogenic, they can still cause anemia, greenish droppings, slight emaciation and reduced egg production [1,59]. Altogether, the infection of birds with these parasites should not be neglected, especially in large commercial poultry production systems.
The present systematic review and meta-analysis have some limitations. Firstly, the heterogeneity among the included studies was high (I2 = 94.81%, 90.4% and 98.8% for the study on Plasmodium (Figure 2), Haemoproteus (Figure 3) and Leucocytozoon (Figure 4), respectively). Heterogeneity might occur due to the varied characteristics of samples or avian species. This was supported by the regression analysis that revealed the significant difference between the prevalence of Plasmodium in wild birds and domestic poultry. Second, the funnel plot and Egger’s test showed publication bias. Thus, this pooled prevalence might be influenced by some small-scale studies. Nevertheless, the prevalence of haemosporidian parasites in Southeast Asia was high, and there were a number of genetic diversities of undescribed species of haemosporidian parasites. In the future, combined microscopic and molecular studies are deemed necessary to explore the actual status of the parasite prevalence. PCR-based (molecular) techniques allow us to understand the genetic characteristics of parasites, which could be used for phylogenetic analysis and the description of lineages following the haemosporidian-specific public database, the MalAvi [9]. However, the microscopy technique was reported as an inexpensive method that can provide an opportunity to determine the identity and intensity of infection [60]. Additionally, the description of parasite morphospecies mainly relied on morphologic characteristics [1,4,5]. Thus, using combined methods might allow the identification of the species, genetic diversity, phylogeny and epidemiology of haemosporidian parasites.

5. Conclusions

The prevalence of haemosporidian parasites, including Plasmodium (21%), Haemoproteus (18%) and Leucocytozoon (34%) was found to be high in Southeast Asia. Generally, domestic poultry has a higher prevalence of Plasmodium than wild birds, demanding continuous monitoring of these parasites in poultry production systems. There were several parasitic lineages of undescribed parasite species found in wild birds, which indicated the existence of overlooked parasites. Further experimental studies using combined microscopic and molecular techniques may reveal such overlooked parasites. Comprehensive knowledge about parasites will help understand host–parasite interactions, pathology and the development of treatment and prevention strategies.

Supplementary Materials

The following supporting information can be downloaded at: https://www.mdpi.com/article/10.3390/ani15050636/s1, PRISMA 2020 checklist. Reference [61] is cited in Supplementary Materials.

Author Contributions

Conceptualization: K.S., N.S. (Nikom Srikacha), S.P., T.M. and P.P.; methodology: K.S., N.S. (Nikom Srikacha), T.M. and P.P.; investigation: K.S, N.S. (Nikom Srikacha), N.S. (Nittakone Soulinthone), W.S., C.J.S., T.M. and P.P.; Visualization: K.S., N.S. (Nikom Srikacha) and P.P.; formal analysis: P.P.; data curation: P.P.; writing—original draft preparation: K.S.; writing—review and editing: N.S. (Nikom Srikacha), N.S. (Nittakone Soulinthone), S.P., W.S., C.J.S. and P.P.; funding acquisition: N.S. (Nikom Srikacha), N.S. (Nittakone Soulinthone), W.S., C.J.S. and P.P.; project administration: P.P. All authors have read and agreed to the published version of the manuscript.

Funding

This work was supported by Walailak University under the New Researcher Development scheme (Contract Number WU67211), the international research collaboration scheme (WU-CIA-04507/2024) and the National Research Council of Thailand (NRCT, Contract Number N42A670081).

Institutional Review Board Statement

Not applicable.

Data Availability Statement

The original contributions presented in this study are included in the article/Supplementary Materials. Further inquiries can be directed to the corresponding author.

Acknowledgments

We would like to thank Akkhraratchakumari Veterinary College, Walailak University, for arranging the “systematic review article workshop”.

Conflicts of Interest

The authors declare no conflicts of interest.

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