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. 2022 Feb 22;17(2):e0264121. doi: 10.1371/journal.pone.0264121

Proportion and seasonality of blood parasites in animals in Mosul using the Veterinary Teaching Hospital Lab data

Hussam M S Alimam 1, Dhiyaa A Moosa 1,#, Eva A Ajaj 1,#, Mohammad O Dahl 1,*, Israa A Al-Robaiee 1,#, Semaa F Hasab Allah 1,2,#, Zahraa M Al-Jumaa 1,#, Eman D Hadi 1,#
Editor: Simon Clegg3
PMCID: PMC8863285  PMID: 35192671

Abstract

Several local studies have examined evidence of blood parasites in different animals in Mosul; however, information about the most prevalent parasite and the seasonality of the infection remains limited. The objective of the study conducted here was to investigate the proportion and seasonality of blood parasites in animals in Mosul using the Veterinary Teaching Hospital Lab data. Laboratory records for a period of 25 months were used for data retrieval. In all included animals, Giemsa-stained blood smears were examined by an attending clinical pathologist for the presence of parasites. Seasons were assigned on a basis of examination date, and the seasonality was quantified by estimating season-to-season ratio. The results indicated that 61.77% of examined animals were tested positive for blood parasites. The most evident parasites were Trypanosoma spp., Theileria spp., Babesia spp., and then Anaplasma spp., with evidence of mixed infection. The odds of the infection did not significantly vary in different age groups. There was a marked linear pattern in the seasonality of the infection with Trypanosoma spp. and Anaplasma spp. An increase of the infection during spring and autumn with Theileria spp. and Babesia spp. was also evident. In conclusion, infection with blood parasites in different animals in Mosul is common with substantial burden, the effect of age-related infection is negligible, and the seasonality of the infection is evident.

Introduction

Blood parasites are frequently diagnosed in different animals examined at the University of Mosul’s Veterinary Teaching Hospital lab. A recent analysis of the records of this hospital indicated that blood parasitic infections constituted the second most frequent cases diagnosed at the hospital, and the most frequent cases in cattle [1]. In a study conducted on 220 cattle from various areas in Mosul, Theileria spp., Babesia spp., Anaplasma spp., Mycoplasma wenyonii, Trypanosoma spp., tachyzoites of Toxoplasma gondii, Microfilaria of Setaria spp., and Ehrlichia spp. were identified in blood smears [2]. Previous studies diagnosed Anaplasma marginale in cows [3], Theileria hirci in local sheep [4], Theileria hirci and Anaplasma ovis in local goats [5], Babesia equi and Babesia caballi in horses [6], and Babesia caballi in camels [7].

Seasonality of blood parasite infection in animals is evident as a function of the seasonal prevalence of the vectors [8]. A recent local epidemiological study indicated that the lowest odds of blood parasites infection were observed in winter, and appeared to be the highest during autumn [1]. Indeed, the prevalence of Trypanosoma spp. is increased three months after the peak of the dry season when the tsetse fly abundance is peaked [9]. During the dry season, adult tsetse flies rely on the blood from the host to adapt to the dry environment [10]. On the other hand, Theileria spp., Babesia spp., and Anaplasma spp. infections are increased with the increase of tick infestation during the rainy season, then summer, and at the lowest rate during winter [11–13].

Information about the proportion and seasonality of blood parasites infection in animals in Mosul is needed. Despite the several studies concerning this type of infection accomplished locally, information about the most prevalent parasite and the seasonality of the infection remains limited. That is, most previous studies such as those by Al-Obaidi and Alsaad [4], Al-Saad and AL-Mola [6], Alsaad et al. [14], and Al-Badrani [15] have focused on studying the clinical and hematological effects of blood parasites on affected animals rather than epidemiological evidence of the infection. Although the study by Al-Abadi and Al-Badrani [2] quantified the proportion of the infection for several parasites, the seasonality was overlooked. In contrast, the study by Dahl et al. [1] calculated the odds of the infection among different seasons without details for each type of parasite. Therefore, the objective of the study conducted here was to investigate the proportion and seasonality of blood parasites in animals in Mosul using the Veterinary Teaching Hospital Lab data. This hospital is one of the main veterinary clinics in Mosul city and receives animals raised in Nineveh governorate, Iraq, particularly Mosul city and its countryside. Records of this hospital have been identified as a source for studying some epidemiological factors of diseases in animals [1].

Materials and methods

Study animals

Animals examined at the University of Mosul Veterinary Teaching Hospital clinical pathology laboratory for evidence of blood parasites in blood smears were considered for inclusion in this study. These animals included cattle, sheep, goats, buffaloes, horses, and dogs. Laboratory records for a period of 25 months (October 30, 2017, to November 30, 2019) were used for data retrieval. Included animals were firstly examined clinically at the hospital’s internal medicine section. Animals that exhibited icteric mucous membranes, enlargement of superficial lymph nodes, hemoglobinuria, tick infestations, and/or prolonged illness were usually considered for further examination via blood smear.

Laboratory examination

Giemsa-stained blood smears were examined under an oil immersion lens by an attending clinical pathologist for the presence of parasites. In this work, different blood parasites were identified as the following (i) Trypanosoma spp. were intercellular elongated and flagellated trypomastigotes, (ii) Theileria spp. were intraerythrocytic round to oval with a nucleus or elongate with bipolar chromatin bodies trophozoites, (iii) Babesia spp. were intraerythrocytic round, ovoid, elongate, or amoeboid trophozoites or pyriform paired merozoites, and (iv) Anaplasma spp. were tiny intraerythrocytic spheres [16].

Data collection

Collected data included: examination date, animal species and age, in addition to results of blood smears. Seasons were assigned on a basis of the examination date. In this study, variables for season and age were identified as previously defined by Dahl et al. [1] as the following: season included winter (1st Dec to 28th Feb); spring (1st March to 31st May); summer (1st Jun to 30th Sept); and autumn (1st Oct to 30th Nov), whereas age included young (< 1-year-old) and adult (≥ 1-year-old). Finally, results of blood smears were identified as positive or negative for Trypanosoma spp., Theileria spp., Babesia spp., and Anaplasma spp., and either single or mixed infection.

Statistical analysis

In this study, the proportion of a particular blood parasite constituted the number of smears tested positive for that parasite to the total number of smears tested positive. The association between the infection and age of the animal was examined via the conditional logistic regression, where the data was matched according to the type of the animal, the odds ratio (OR) was considered to measure the magnitude of the association, and value of P ≤ 0.05 (two-tailed) was considered significant [17]. On the other hand, the seasonality was measured via a direct comparison between the proportions of a particular parasite infection among different seasons [18]. In addition, the seasonality was quantified by estimating season-to-season ratio taking into consideration differences in the length of each season using an equation adapted from Ferreira et al. [19] as the following: S1-to-S2 ratio = (P1/S1length)/(P2/S2length), where;

  • S1 = season one (e.g., spring),

  • S2 = season two (e.g., summer),

  • P1 = proportion of a particular parasite detected during season one,

  • P2 = proportion of a particular parasite detected during season two,

  • S1length = length of the season one in days,

  • S2length = length of the season two in days,

Results

Among 552 blood smears were examined, 341 (61.77%) were tested positive for blood parasites from different animals. Generally, Trypanosoma spp. was the most reported blood parasite, followed by Theileria spp., Babesia spp., and then Anaplasma spp. (Fig 1). In this data, Trypanosoma spp. was the most evident blood parasite in ruminants (cattle, sheep, goats, and buffalo), Theileria spp. was frequently reported in all tested animals except dogs, Babesia spp. constituted the most blood parasite diagnosed in blood smears from dogs, and Anaplasma spp. was detected in cattle only (Table 1). Mixed infection with at least two types was reported in only 4.5% of the positive cases (Fig 2). Additionally, although the differences in the proportion of the infection by Trypanosoma spp. was more than 10% greater in young compared to adult animals (44.87%– 34.39% = 10.48%), the odds did not reach the assigned statistical significance (P-value = 0.09; Table 2). On the other hand, the differences in the proportion of infection by Anaplasma spp., Babesia spp., and Theileria spp. among young and adult animals were not significant (P-values > 0.05; Table 2).

Fig 1. The proportion of blood parasites detected in blood smears from animals tested at the Veterinary Teaching Hospital | University of Mosul between Oct 30, 2017 to Dec 31, 2019.

Fig 1

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Table 1. Distribution of blood parasites according to the type of animal using blood smears tested at the Veterinary Teaching Hospital | University of Mosul between Oct 30, 2017 to Dec 31, 2019.

Tested Animals Trypanosoma Theileria Babesia Anaplasma
Type N +ve n (%) n (%) n (%) n (%)
Cattle 351 223 128 (57.40) 83 (37.22) 10 (4.48) 20 (8.97)
Sheep 114 77 49 (63.64) 23 (29.87) 9 (11.69) 0
Goats 22 15 8 (53.33) 5 (33.33) 2 (13.33) 0
Buffalo 28 15 11 (73.33) 6 (40) 1 (6.67) 0
Horse 19 5 1 (20) 2 (40) 2 (40) 0
Dog 18 6 1 (16.67) 0 5 (83.33) 0
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Abbreviations: (N): total number of tested animals, (+ve): number of animals with blood smear tested positive for at least one type of blood parasite, (n): number of animals tested positive for a particular parasite, and (%): proportion of a particular parasite among positive blood smears for the same type of animal.

Fig 2. The proportion of mixed infection with blood parasites among positive blood smears.

Fig 2

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Table 2. The proportion of blood parasites infection according to the age of the animal and the conditional logistic regression for the odds of the infection in adults compared to young animals.

Parasite | Age Tested Animals Proportion of infection OR 95% CI P
Positive N = 78 Negative N = 474
Trypanosoma
 Young 35 43 44.87% 1.00 Referent1 NA
 Adult 163 311 34.39% 0.65 0.39, 1.08 0.09
Theileria
 Young 19 59 24.36% 1.00 Referent1 NA
 Adult 100 374 21.10% 0.94 0.53, 1.69 0.84
Babesia
 Young 2 76 2.56% 1.00 Referent1 NA
 Adult 27 447 5.70% 1.24 0.27, 5.77 0.78
Anaplasma *
 Young 2 76 2.56% 1.00 Referent1 NA
 Adult 18 456 3.80% 2.54 0.58, 11.19 0.22
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* Cattle only.

1Referent: a category of comparison for the other category.

Abbreviations: (OR): odds ratio, (CI): confidence interval.

The results revealed that there was an evident pattern in the seasonality of the infection (Fig 3, Table 3). In Trypanosoma spp. infection, there was linear increase in the percentage of the infection from spring to autumn to be declined in winter. On the other hand, infections with Theileria spp. and Babesia spp. slightly increased in spring and autumn compared to summer, while markedly decreased during winter. Finally, there was linear decrease in the percentage of the infection with Anaplasma spp. during the year from spring to winter.

Fig 3. Seasonality of blood parasites detected in blood smears.

Fig 3

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Table 3. Season-to-season ratio as a measure of seasonality of the infection percentage according to the type of blood parasite.

Season-to-season ratio Trypanosoma Theileria Babesia Anaplasma
Spring to summer ratio 0.83 1.49 2.05 2.88
Summer to autumn ratio 0.45 0.48 0.36 1
Autumn to winter ratio 2.14 2.80 3.52 NA
Winter to spring ratio 1.23 0.49 0.39 NA
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Discussion

The study conducted here revealed that Trypanosoma spp. was the most evident blood parasite diagnosed in the animals in Mosul, followed by Theileria spp. In addition, Trypanosoma spp. was mostly reported during autumn, whereas both Theileria spp. and Babesia spp. were mostly reported during spring and autumn. The current study is considered the first study in Mosul city that examined the seasonality of blood parasites in animals. Our data for two successive years enabled us to better examine the seasonality of the reported blood parasites.

In this study, 61.77% of blood smears tested positive for blood parasite. This percentage is considered relatively high and indicates that the infection rate of blood parasites in animals in Mosul is substantial. The most prevalent parasite reported here was Trypanosoma spp. For the first time in Mosul, Trypanosoma vivax was diagnosed by Rhaymah and AL-Badrani [20] in blood smears from imported calves, Trypanosoma congolense was identified by Hasan [21] in cattle and sheep, Trypanosoma brucei was detected by Al-Badrani [15] in cattle. Subsequently, Trypanosoma spp. was diagnosed in 6.5% of positive blood smears of cattle in Mosul, as the fourth most frequent blood parasite [2]. It seems that this infection has emerged to the city around 2011 as a result of uncontrolled importation [15, 20, 21], and then widely spread between local animals to become the most frequent blood parasite infection diagnosed in blood smears in the current investigation. More epidemiological research is important to identify its vectors, sources of infection, and risk factors in the city.

The study reported here revealed that Theileria spp. is a common blood parasite in local animals. The parasite has been diagnosed in several previous local studies in different animals. For instance, Theileria hirci was identified by Al-Obaidi and Alsaad [4] and Al-Obaidi [5] in local sheep and goats, respectively. In addition, Theileria camelensis was detected by Al-Saad et al. [22] in camels, and Theileria annulata was revealed by Alsaad et al. [14] in blood smears from newborn calves. Therefore, Theileria spp. is considered an endemic parasite in the area, and a percentage of about 35% among positive blood smears is considered high. Studies about the prevalence of Theileria spp. in animals in Mosul are very limited. The only available percentage of Theileria spp. infection among other blood parasites in cattle is 15.78% [2], which is lower than that reported in our study here, reflecting poor or ineffective control measures against the parasite and its vector.

In this study, Babesia spp. was reported at 8.4% among other blood parasites. This parasite has been identified in several previous studies, such as Babesia equi and Babesia caballi in horses [6, 23], Babesia motasi, Babesia ovis, B. motasi, B. foliate, and B. taylori in goats [14, 24], Babesia bovis, B. bigemina, and B. divergens in cattle [2, 25], and Babesia caballi in camels [7]. Studies about the prevalence of Babesia spp. in animals in Mosul are also very limited. The only available percentage of Babesia spp. infection among other blood parasites in cattle is 10% [2], which is higher than that reported in our study here. It is difficult to consider that the prevalence of Babesia spp. in animals in Mosul city has decreased because the available prevalence by Al-Abadi and Al-Badrani [2] was for cattle only. More epidemiological surveys are required to confirm this finding.

The study conducted here revealed that Anaplasma spp. was diagnosed in blood smears from cattle only. In Mosul, however, Anaplasma marginale has been identified in buffalo [26], camel [27], while Anaplasma ovis was detected in goats [5, 14], in addition to that reported in cattle [3, 28]. Nevertheless, no previous study has reported the percentage of infection among other blood parasites except that for Al-Abadi and Al-Badrani [2] in cattle at 4.4%, which is lower than that reported in the study conducted here. An increase in the percentage of the infection is probably due to the absence of an effective control program against the parasite and its vector. Additionally, careful examination to blood smears from animals other than cattle is important as it was previously reported in goats, buffalo, and camels.

Results of the current data revealed that mixed infection is evident. This result is in line with the study of Al-Abadi and Al-Badrani [2] who reported mixed infection of blood parasites in cattle in Mosul. The presence of mixed infection with blood parasites is not unusual and is reported by other studies [29, 30]. On the other hand, our result showed no difference in the odds of the infection in adult animals compared to young. The current study cited eighteen local studies examined blood parasites in different animals [2–7, 14, 15, 20–28], however; none of them have reported the difference in the percentage of the infection among adults compared to young. Vieira et al. [30] did not show a difference in the percentage of the animals infected with Babesia spp. between different age groups, in contrast to that for Anaplasma marginale. It seems that the vector can infect adults as same as young animals; therefore, the odds of the infection are potentially not different.

The study reported here indicated seasonal differences in the infection. Our study is considered the first local study that examined the seasonality of the infection with blood parasites among animals. The seasonality of blood parasite infection in animals is evident as a function of the seasonal prevalence of the vectors [8]. Our results are in line with the study of Nnko et al. [9] who indicated that the infection with Trypanosoma spp. increases after the peak of the dry season by about three months. On the other hand, our study showed that the infection with Theileria spp., Babesia spp. increased during spring and autumn, which is in line with studies of, Asmaa et al. [11], Ayadi et al. [12], and Lempereur et al. [13]. Moreover, season-to-season ratio that took into account the difference in the length of the season confirmed the pattern of the seasonality observed by the percentage. Finally, additional studies are required to confirm these findings in local animals.

Conclusions

The study concluded that the infection with blood parasites in different animals in Mosul is common with relatively high infection rate, the effect of age-related infection is negligible, and the seasonality of the infection is evident. Missing season-related investigations in the previous years could contribute to the endemic situation of the infection in the city. More epidemiological studies are required in order to outline control strategies against such infections.

Acknowledgments

The authors thank the College of Veterinary Medicine, University of Mosul, for supporting this work.

Data Availability

All relevant data are within the paper.

Funding Statement

The author(s) received no specific funding for this work.

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PONE-D-21-39858Proportion and Seasonality of Blood Parasites in Animals in Mosul using the Veterinary Teaching Hospital Lab DataPLOS ONE

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4. Is the manuscript presented in an intelligible fashion and written in standard English?

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Reviewer #1: Yes

Reviewer #2: No

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5. Review Comments to the Author

Please use the space provided to explain your answers to the questions above. You may also include additional comments for the author, including concerns about dual publication, research ethics, or publication ethics. (Please upload your review as an attachment if it exceeds 20,000 characters)

Reviewer #1: This is an interesting epidemiological survey that provides new insights into the seasonality of infections caused by blood-borne pathogens in the animals of Mosul. I only have some minor suggestions for improvement, which are below, but other than that, I think it largely reads well!

1. In general, I would suggest changing "blood parasites" to "blood pathogens" or something that covers bacteria as Anaplasma, Ehrilichia, etc are not specifically parasites, even though some consider them as such.

I would also italicize any "et al" when referencing authors.

2. In your title, it may beneficial to specify what animals you examined, maybe "...livestock and dogs in Mosul..."?

3. In line 45 of your introduction, it should say "blood parasitic (or pathogenic if you change it) infections constituted..." and in line 68, it should say "such as those by Al-Obaidi...".

4. In your methods, I would recommend mentioning what animals you examined or refer to Table 1.

In line 90, it should be "tick infestations" and in your Laboratory Examination paragraph, it should read "Trypanosoma spp. were intercellular..." and the same for the other pathogens. In line 109-110, it should say "...and either single or mixed...".

I am also just curious, was there a reason the abundance (or number) of parasites/bacteria in each blood smear was not examined?

5. In your results, I would add the total number of samples examined between "...341 blood smears" and "(61.77%)...".

Line 143-144 should say "Additionally, the differences in the proportion...".

I would also only have "...at the Veterinary Teaching Hospital | University of Mosul between Oct 30, 2017 to Dec 31, 2019" on the first caption rather than each one.

Also can you explain what "Referent" means under 95% CI in Table 2?

6. In your discussion, line 198 should read "...city to examine..." and line 201 should say "...blood parasites".

In line 202, I would maybe change "burden" to "infection rate" as that sounds more like abundance.

In line 229-230, I would change it to read "[6, 23], Babesia ovis, B. motasi, B. foliate, and B. taylori in goats [14, 25]...".

Line 239-241 would be better as "...Anaplasma marginale has been identified in buffalo [27], camel [28] while Anaplasma ovis was detected in goats [5, 14] in addition to that reported in cattle...".

There should be an author referenced in line 242 and 249 after "for [2]" and "of [2]' and some references in line 247 after "...camels".

Line 252 should be "adult animals..." and in line 253, it should be "On the other hand, nineteen..."

Line 254 should read "...animals [reference]; however,..." and line 258, it should be "...adults as well as young...".

7. In your conclusion, I would again change "...substantial burden" to something like "a relatively high infection rate" in line 274.

Line 276-277 should be "...endemic understanding of the infection..."

8. Your tables and figures mostly look good but in Figure 3, Theileria is misspelled and I wonder if it also needs standard error/deviation bars?

I hope these suggestions help make minor improvements but it is a very fascinating paper otherwise!

Reviewer #2: Summary of the research:

I have summarised that the main research question for this journal entry is whether the time of year directly influences parasitic burdens within animals (cattle, sheep, goats, buffalo, horses, and dogs) that have been previously admitted to a Veterinary teaching hospital in Mosul, Iraq. This study also selected to focus on whether there was an association between age, seasonality, and parasitic burden. The research focuses on the detection of blood parasites (Trypanosoma spp., Theileria spp., Babesia spp. and Anaplasma spp., this also includes mixed infections) from Giemsa-stained smears and microscopy which remains the ‘Gold Standard’ tool of identification for blood parasite, and I therefore believe is accurately researched and reported. Within the study, the examination dates were the dates used to assign seasonality to each sample. It is stated that prior studies from Mosul involving blood parasites have been undertaken, however, an association with seasonality has been previously overlooked and is thus a gap in knowledge.

What are the claims and conclusions made in this study?

This study claims there is a relationship between seasonality and parasitic infections based on the season-to-season ratio adapted from Ferreira et al. The literature claims that Trypanosoma, Theileria and Babesia all peak in the Autumn-Winter ratio. They claim that Anaplasma has only been found predominantly within cattle samples, and this infection peaks in the Spring to Summer ratio, but there is no found evidence of the parasite occurring from Autumn to Winter or Winter to Spring ratios. It was also claimed that dogs predominantly harboured Babesia spp. They concluded that there is no significance between parasitic burden and age.

What is the relevancy, and does it fit with the existing literature?

I believe that the investigation, monitoring and understanding of animal parasites are a key part of improving veterinary care, medicine, and infection control measures; this can be used for preventative measures, emergency outbreaks, it can aid how animal husbandry may need to be altered to protect animal welfare and likewise, humans. It does fit with existing literature, since there is already published reports regarding the parasitic burden within Mosul, this piece of literature fills a gap in knowledge surrounding a correlation with seasonality which is an essential factor of the prevalence of parasites dependant on their life cycles, their environment and the animals present in these environments; this can aid/drive prevention and future parasite control in Mosul.

Minor Issues:

• Formatting issues (figures do not line up with the formatting e.g. Page 8, Fig 1. Page 9, Fig 2 and Page 11, Fig 3.)

• There is no mention of n (total sample size) analysed within the study animals/data collection section.

• Page 12, line 209: ‘it seems that this infection has emerged to the city around 2011’, this statement has no reference or further information to support the claim being made.

• Page 11, line 198, this does not read correctly and has grammatical issues.

• Page 12, line 201 ‘relatively considered high’, requires rewording.

• Page 14, line 235 ‘in Mosul in animal has’, grammatical issue.

• Page 15, line 260 ‘examined’ requires grammatical correction.

• Page 11, line 179 ‘increase in the in’ grammatical issue.

• Page 10, line 170 ‘the proportion of blood parasites infection’

Major Issues:

• Criterion of examining certain blood samples only from symptomatic (icteric mucous membranes, enlargement of superficial lymph nodes, haemoglobinuria, ticks, and prolonged illness) animals, has potentially limited the true reflection of parasitic infection prevalence within Mosul; therefore also limiting the true reflection of seasonal parasitic infections as only clinically unwell animals are examined microscopically due to circumstances of being brought to the Veterinary Hospital and blood taken under these animals meeting these conditions. Low burden parasitic infections can be asymptomatic, and equally, parasites are still found in clinically healthy animals, including cattle (example: https://parasitesandvectors.biomedcentral.com/articles/10.1186/s13071-016-1498-1).

• Total sample size is 552 animals. A larger sample size may have benefited this study and increased reliability of results and therefore the conclusions that can be drawn from a larger data set, by including animals that do not visually manifest a certain set of criteria. This can eliminate bias (only including animals manifesting certain symptoms) and more asymptomatic cases and low parasitic burdened animals could be found and may offer more data.

• The data used to ‘assign’ seasonality (Winter: 1st December to 28th February. Spring: 1st March to 31st May. Summer: 1st June to 30th September and Autumn: 1st October to 30th November) was stated as the examination date, not the sample collection date. This has the potential to be inaccurate due to possible delayed examinations and other circumstances that can delay the process of identification; unless otherwise stated that the examination date and collection date are equivalents, and do not differ. Is the examination date the same as the collection date of the original sample?

Additional comments:

A thoroughly intriguing study and I enjoyed reading it. This research fills an important gap within knowledge concerning parasitic burden in animals within Mosul, and it is a key element that can not be overlooked for animal and human health, with good reason. I would be happy to review this paper again.

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Reviewer #2: No

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PLoS One. 2022 Feb 22;17(2):e0264121. doi: 10.1371/journal.pone.0264121.r002

Author response to Decision Letter 0

31 Jan 2022

The authors thank the reviewer for the review and critique of this manuscript. As a result, the authors have produced a better manuscript. A response to each point raised by the reviewers is included in the attached file.

Attachment

Submitted filename: Response to Reviewers.docx

Click here for additional data file. (37.1KB, docx)

Decision Letter 1

Simon Clegg

4 Feb 2022

Proportion and Seasonality of Blood Parasites in Animals in Mosul using the Veterinary Teaching Hospital Lab Data

PONE-D-21-39858R1

Dear Dr. Dahl,

We’re pleased to inform you that your manuscript has been judged scientifically suitable for publication and will be formally accepted for publication once it meets all outstanding technical requirements.

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Additional Editor Comments:

Many thanks for resubmitting your manuscript to PLOS One

As you have addressed all the comments and the manuscript reads well, I have recommended it for publication

You should hear from the Editorial Office shortly.

It was a pleasure working with you and I wish you the best of luck for your future research

Hope you are keeping safe and well in these difficult times

Thanks

Simon

Acceptance letter

Simon Clegg

9 Feb 2022

PONE-D-21-39858R1

Proportion and Seasonality of Blood Parasites in Animals in Mosul using the Veterinary Teaching Hospital Lab Data

Dear Dr. Dahl:

I'm pleased to inform you that your manuscript has been deemed suitable for publication in PLOS ONE. Congratulations! Your manuscript is now with our production department.

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on behalf of

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Academic Editor

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