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Basic routes of transmission of respiratory pathogens—A new proposal for transmission categorization based on respiratory spray, inhalation, and touch
Indoor Air ( IF 5.8 ) Pub Date : 2021-01-21 , DOI: 10.1111/ina.12786
Yuguo Li 1
Affiliation  

A primary challenge in combatting the ongoing coronavirus disease 2019 (COVID‐19) pandemic is to clarify the definitions and roles of airborne transmission, contact transmission, and droplet transmission of the causative agent, severe acute respiratory syndrome coronavirus 2 (SARS‐CoV‐2).1 Confusion about these key aspects exists among both the general population, who are interested in evaluating their own infection risk in different settings, and scientists of different disciplines. Debate over these definitions continues,2 with many questions, such as the following, being asked. What is the difference between airborne transmission and aerosol transmission? What is the droplet threshold size in droplet transmission? What is the difference between transmission by fomites (contaminated inanimate surfaces or objects) and transmission by contact? If fomite transmission can occur, is transmission from animate surfaces also possible?

There are various definitions for the different routes of transmission of respiratory pathogens (typically viruses), and at least three routes are currently thought to play a role, according to the World Health Organization (WHO)3 and the US Centers for Disease Control and Prevention (US CDC).4 Here, we adopt the following definitions from Shiu et al.1 for discussion.

  1. Contact transmission involves the transfer of virus‐laden respiratory secretions from an infected person to a susceptible person, either directly (via physical contact) or indirectly (via surfaces or objects).
  2. Large‐droplet or droplet transmission involves the expulsion of virus‐laden respiratory droplets from an infected person and the subsequent deposition of these droplets on the mucosal surfaces (eg, eyes, nose, and mouth) of a susceptible person.
  3. Airborne or aerosol transmission involves virus‐laden fine, airborne respiratory droplets being generated by the exhalation of an infected person, or by a medical aerosol‐generating procedure being performed on an infected person, and these droplets subsequently being inhaled by a susceptible person.

Among these, the definition of contact transmission appears to be the most confusing. The term “contact” refers to both direct physical contact between the infected and the susceptible persons, and indirect contact via the touching of intermediate surfaces or objects. The latter is also called the fomite route. The term “intermediate” implies that the surfaces or objects lie “between” the infected and the susceptible persons, that is, the surface or object is contaminated by the infected person, prior to the surface being touched by the susceptible person. However, a surface may also be contaminated by a healthy person's hands in a surface touch network.5 In addition, the word “contact” can be inferred to mean physical or social contact, which may lead to confusion over the exact definitions of contact transmission. In physical terms, aerosol transmission is also a form of indirect contact via air, while large‐droplet transmission is also a form of indirect contact. The term “droplet transmission” is also confusing, as it implies that all droplets are large and will deposit on mucosal surfaces. Finally, the short‐range aerosol route is not considered, as the aerosol transmission route refers only to long‐range aerosol transmission. In fact, short‐range and long‐range aerosol transmission should not fall under the same category, as they are prevented by different measures. Thus, short‐range aerosol transmission should be considered a type of close‐contact transmission, together with large‐droplet and direct‐contact transmission.

If we consider that categorization is a way to sort different transmission events into groups based on different criteria, then those used for categorizing the three traditional categories of transmission routes appear unclear. We have attempted to use a transmission media–based approach to clarify the existing categorization of the routes of transmission of respiratory pathogens.6 In reality, there may be multiple layers of intermediate transmission media. Expired droplets are the primary carriers of pathogens after their release from infected persons. Once expired droplets are deposited on or transferred to an inanimate surface or object (fomite), fomites are the transmission media. However, animate surfaces, such as hands and faces, can also be media in indirect transmission, and hands are essential media for fomite transmission. Droplets are transmission media in nearly all of the routes, except for the direct transfer of bodily fluids containing pathogens, for example, via kissing. Air itself cannot transmit pathogens if air does not flow or is not inhaled. Thus, if the transmission media–based criterion is used, aerosol transmission appears to be a better definition than airborne transmission.

It is useful to briefly consider the history of the concept of pathogen transmission, as the concepts we use today are based on those established at the dawn of modern science, and it is to be expected that these concepts will evolve with our understanding of the underlying science. Girolamo Fracastoro (1476–1553) “defined a contagion as a precisely similar corruption, developing in the substance of a combination of elements, which passed from one thing to another and was the result of an infection first occurring in the imperceptible particles. There were three different types of contagion, by direct contact, by contact leaving behind ‘fomites’ that preserved the seeds of contagion and [were] infected by them; and at a distance as if by some impetus or poison. In all three, infection was produced not by an unknown ‘occult’ cause, but by seeds (semina, seminaria) of contagion, which varied with the type.”7 Fracastoro also speculated upon the concept of airborne seeds (or “seedlets” of contagion). However, the erroneous “miasma” theory of pathogen transmission continued to dominate, and Fracastoro's “seed of disease” contagion theory was not accepted until the development of germ theory by Louis Pasteur (1822–1895) and Robert Koch (1843–1910). Pasteur also discovered that microbes were present in air.8

Carl Flügge (1847–1923) and others first conceptualized the large‐droplet transmission route9 and observed that the organisms in the expired droplets could not be recovered by sampling plates exposed at distances beyond 1–2 m from the infectious person. Charles Chapin (1856–1941)9 established that contact transmission is the dominant route of transmission of infection pathogens. He wrote that “Infection by air, if it does take place, as is commonly believed, is so difficult to avoid or guard against, and so universal in its action, that it discourages effort to avoid other sources of danger. If the sick‐room is filled with floating contagium, of what use is it to make much of an effort to guard against contact infection? If it should prove, as I firmly believe, that contact infection is the chief way in which the contagious diseases spread, an exaggerated idea of the importance of airborne infection is most mischievous.” William Wells developed the concept of droplet nuclei and a relatively modern theory of airborne transmission.10 However, it is often overlooked that he also calculated and suggested that the droplet threshold size was “a tenth of a millimeter” (ie, 100 µm).10

As reviewed in,6 Garner11 was probably the first to suggest the involvement of droplets larger than 5 µm in large‐droplet transmission and to pioneer the concept of transmission‐based precautions against droplet, contact, and inhalation transmission. The 2014 WHO guidelines3 define droplets as “respiratory aerosols >5 µm in diameter.” However, the threshold diameter is much larger (50–100 µm), as can be shown by calculating the probability of deposition of an expired droplet.6, 12 A drop falls (drops) due to its own weight, while a droplet is a very small drop that does not fall easily. The ability for a droplet to become suspended in air also depends on surrounding airflows, with larger droplets being suspended by stronger airflows. This may have a large effect on airborne transmission, given the difference is size between droplets in a jet expired during normal exhalation, at a typical speed of 2 m/s, with those released in a cough, at a typical speed of 20 m/s, into a typical room airflow speed of <0.25 m/s. Thus, it may be better to simply refer to drops rather than large droplets and to use aerosols to refer to droplets that are small enough to remain suspended in air for a certain period of time. It is notable that aerosols in room air are mostly 5 µm or less in diameter, while those in expired jets are much larger (≤50 µm in diameter12).

As a side note, both the WHO and the US CDC consider that precautions against the transmission of respiratory pathogens include those that guard against contact, droplet, and airborne transmission and that these should be implemented in addition to standard precautions.3, 4 It is typically stated that it is more important to implement several of these precautions rather than an individual precaution, which attests to the likelihood that multiple routes of transmission can operate, that there is uncertainty over which transmission routes are most prominent, and that there is some ambiguity in the definitions of the routes of transmission. It would therefore be helpful if the routes of transmission could be defined more explicitly, such that more exact precautions could be taken.

The classical categorization as described above is conceptually useful, but it is based on imagination and reasoning, rather than a systematic consideration of the categorization criteria. The new knowledge that has been gained on the generation, release, transport, and routes of exposure to respiratory droplets enables the revision of this categorization. A good categorization of transmission routes should be free of ambiguity or inconsistencies, such that public health experts can develop consistent precaution and prevention policies, and that researchers of multiple disciplines can easily apply and integrate their knowledge into the study of transmission mechanisms and interventions. Transmission route categorizations should also be updated in response to the latest mechanistic understandings on transmission mechanisms, rather than attempting to fit this new knowledge into the existing definitions, as was done during the development of the short‐range aerosol transmission route and the surface touch network transmission routes.

The existing concepts of aerosol, fomite, and large‐droplet transmission are based on where pathogenic particles are positioned (ie, in the air, on fomites, or in/or droplets), not how they are transferred (transmitted). Both large‐droplet transmission and close‐contact transmission were proposed before the theory of air jets was developed, and the latter has now been widely used to understand the airflows expired during respiratory activities, such as coughing and normal breathing. Furthermore, the concept of airborne transmission of droplet nuclei10 was developed well before it was possible to distinguish air‐distribution patterns in buildings.

Below, we suggest a set of transfer process–focused criteria for categorizing the basic routes of transmission of respiratory viruses. The media involved are shown in brackets, and we adopt a “media + transfer” structure in this new categorization.

  1. (Drop) spray transmission refers to respiratory viruses that are transmitted by the spray of virus‐laden drops expelled from an infected person being deposited on the mucosal surfaces (eg, eyes, nose, and mouth) of a susceptible person. Thus, only drops that move can transmit a virus by this process, where this movement is due to the momentum gained at the point of release, for example, at the mouth. Due to the nature of expired airflows, such drop spray transmission will only be possible within a certain proximity. Chapin9 wrote that “most diseases are not likely to be dust‐borne, and they are spray‐borne only for two or three feet, a phenomenon which, after all, resembles contact infection more than it does aerial infection as ordinarily understood.” Drop spray transmission is identical to traditional large‐droplet transmission, but avoids the use of the ambiguous “droplets” term, and the word “spray” enhances understanding: It is easy to visualize a face shield being used to block a spray, or a face mask being used to block drops.
  2. (Aerosol) inhalation transmission refers to air‐suspended virus‐laden respiratory droplets being exhaled by an infected person and inhaled by a susceptible person. Aerosol inhalation can occur over the short range and long range. The risk of transmission by aerosol inhalation is greater when a susceptible person is in close proximity to an infected person, that is, within 1–2 m. Flowing air can transport respiratory aerosols around, but unmoving air cannot. However, a person may inhale virus‐containing aerosols from a room containing unmoving air, as inhalation is itself an airflow process.
  3. (Surface) touch transmission refers to animate (eg, skin) or inanimate (fomite) surface‐dwelling virus‐laden respiratory drops or droplets being transferred by a person hand touching such a surface and subsequently touching his/her mucosa, resulting in self‐inoculation.

These three newly defined routes may be considered as the three basic viral transmission routes. Obviously, the fourth transmission route is the direct transfer of bodily fluids containing pathogens (eg, kissing). While spray transmission can only occur during close contact, both inhalation and touch transmission can occur over a long distance. These three basic transmission processes also satisfy one of the basic principles of categorization, that is, cognitive economy, which means “to provide the maximum information with the least cognitive effort.”13 These processes may be adaptable to categorize transmission of aerosols generated by other mechanisms (eg, medical aerosols or fecal aerosols), if they are shown to play a role in the transmission of a specific pathogen.

It may be possible to further classify the transmission routes according to common relations or attributes, such as infection settings, distances between the infected and the susceptible persons, transmission media, or the origin of virus‐laden droplets or aerosols.

With respect to distance, there are two types of transmission: close‐contact transmission (proximity or short distance, ie, within 1–2 m from the infected person) and distant transmission (long distance, ie, >1–2 m from the infected person) (Figure 1). Crucially, our definitions clarify that all three basic routes of virus transmission, that is, spray, inhalation, and touch transmission, can be involved in close‐contact transmission. Proximity inhalation transmission has been referred to as “short‐range aerosol transmission” in the literature, while proximity touch transmission has been denoted as the “immediate surface” route.6 However, with respect to close‐contact transmission, the US CDC and WHO transmission‐based precaution approach3, 4 does not consider the proximity inhalation route, despite this being likely to occur and possible dominates. Inhalation and touch‐based transmission are both possible forms of distant transmission. Finally, aerosols involved in proximity inhalation are larger than those involved in distant inhalation.

image
FIGURE 1
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An illustration of the three basic short‐distance transmission routes—spray, inhalation, and touch—and long‐distance transmission (inhalation and touch) in a room. The expired jet range is shown in light green, the infected person is shown in red, and the susceptible person is shown in blue (modified from14). The drops are shown as large black circles, and the aerosols, as small black circles


中文翻译:

呼吸道病原体的基本传播途径——基于呼吸道喷雾、吸入和接触的传播分类新建议

与正在发生的 2019 年冠状病毒病 (COVID-19) 大流行作斗争的一个主要挑战是阐明病原体、严重急性呼吸系统综合症冠状病毒 2 (SARS-CoV-2) 的空气传播、接触传播和飞沫传播的定义和作用)。1对评估自己在不同环境中的感染风险感兴趣的普通人群和不同学科的科学家都对这些关键方面存在困惑。关于这些定义的争论仍在继续,2提出了许多问题,例如以下问题。空气传播和气溶胶传播有什么区别?液滴传输中的液滴阈值大小是多少?污染物(受污染的无生命表面或物体)传播与接触传播有什么区别?如果可以发生污染物传播,是否也可以从有生命的表面传播?

根据世界卫生组织 (WHO) 3和美国疾病控制与预防中心的说法,呼吸道病原体(通常是病毒)的不同传播途径有多种定义,目前认为至少有三种途径起作用(美国疾控中心)。4在这里,我们采用 Shiu 等人的以下定义。1供讨论。

  1. 接触传播涉及将携带病毒的呼吸道分泌物从感染者直接(通过身体接触)或间接(通过表面或物体)转移到易感者。
  2. 大飞沫或飞沫传播包括从感染者身上排出携带病毒的呼吸道飞沫,随后这些飞沫沉积在易感者的粘膜表面(例如,眼睛、鼻子和嘴巴)上。
  3. 空气传播或气溶胶传播涉及由感染者呼气或对感染者进行医疗气溶胶生成程序产生的携带病毒的细小空气传播飞沫,然后这些飞沫随后被易感者吸入。

其中,接触传播的定义似乎最为混乱。术语“接触”是指感染者和易感者之间的直接身体接触,以及通过接触中间表面或物体的间接接触。后者也称为 fomite 路线。术语“中间”意味着表面或物体位于感染者和易感者“之间”,即在易感者接触表面之前,表面或物体已被感染者污染。然而,在表面触摸网络中,表面也可能被健康人的手污染。5此外,“接触”一词可以推断为身体或社会接触,这可能会导致对接触传播的确切定义的混淆。从物理上讲,气溶胶传播也是通过空气间接接触的一种形式,而大液滴传播也是一种间接接触形式。术语“飞沫传播”也令人困惑,因为它意味着所有飞沫都很大并且会沉积在粘膜表面。最后,不考虑短程气溶胶传播途径,因为气溶胶传播途径仅指远程气溶胶传播。事实上,短程气溶胶传播和长程气溶胶传播不应属于同一类别,因为它们的预防措施不同。因此,短距离气溶胶传播应被视为一种密切接触传播,

如果我们认为分类是根据不同的标准将不同的传播事件分类成组的方法,那么用于对三种传统传播途径进行分类的方法就显得不清楚了。我们尝试使用基于传播媒介的方法来阐明呼吸道病原体传播途径的现有分类。6实际上,中间传输介质可能有多层。过期的飞沫从感染者身上释放出来后,是病原体的主要携带者。一旦过期的液滴沉积或转移到无生命的表面或物体(污染物)上,污染物就是传输介质。然而,有生命的表面,例如手和脸,也可以是间接传播的媒介,而手是污染物传播的基本媒介。飞沫是几乎所有途径的传播媒介,除了含有病原体的体液的直接转移,例如通过接吻。如果空气不流动或不被吸入,空气本身就不能传播病原体。因此,如果使用基于传输介质的标准,气溶胶传输似乎是比空气传播更好的定义。

简要考虑病原体传播概念的历史是有用的,因为我们今天使用的概念是基于现代科学初期建立的概念,预计这些概念将随着我们对基本原理的理解而发展科学。Girolamo Fracastoro(1476-1553)“将传染病定义为一种完全相似的腐败,在元素组合的物质中发展,从一个事物传递到另一个事物,并且是首先发生在难以察觉的粒子中的感染的结果。有三种不同类型的传染病,通过直接接触,通过接触留下“污染物”来保存传染病的种子并[被]感染;并且在远处仿佛受到某种推动或毒药的影响。在所有三个中,感染不是由未知的“神秘”原因引起的,而是由种子引起的(seminaseminaria)传染,它与类型而变化的“。7 Fracastoro 还推测了空气传播的种子(或传染的“种子”)的概念。然而,病原体传播的错误“瘴气”理论继续占主导地位,直到路易斯巴斯德(1822-1895)和罗伯特科赫(1843-1910)细菌理论的发展,弗拉卡斯托罗的“疾病种子”传染理论才被接受。巴斯德还发现空气中存在微生物。8

Carl Flügge (1847-1923) 和其他人首先将大飞沫传播途径9概念化,并观察到在距离感染者 1-2 m 的距离外对暴露的平板进行采样时,无法回收呼出的飞沫中的生物体。查尔斯·查平 (1856–1941) 9确定接触传播是感染病原体的主要传播途径。他写道:“空气感染,如果确实发生了,正如人们普遍认为的那样,很难避免或防范,而且其作用如此普遍,以至于不鼓励避免其他危险源的努力。如果病房里到处都是漂浮的传染病,那么努力防范接触感染又有什么用呢?如果它如我坚信的那样证明接触感染是传染病传播的主要方式,那么夸大空气传播的重要性的想法是最恶作剧的。” 威廉威尔斯发展了液滴核的概念和相对现代的空气传播理论。10然而,经常被忽视的是,他还计算并建议液滴阈值尺寸为“十分之一毫米”(即 100 µm)。10

正如6 Garner 11所评论的,可能是第一个提出大于 5 µm 的飞沫参与大飞沫传播的人,并开创了基于传播的预防飞沫、接触和吸入传播的预防措施的概念。2014 年世卫组织指南3将飞沫定义为“直径 >5 µm 的呼吸道气溶胶”。然而,阈值直径要大得多 (50–100 µm),这可以通过计算过期液滴的沉积概率来显示。6、12水滴因自身重量而下落(下落),而水滴是非常小的水滴,不易下落。液滴悬浮在空气中的能力还取决于周围的气流,较大的液滴被更强的气流悬浮。这可能对空气传播产生很大影响,因为在正常呼气时喷出的液滴之间的大小不同,典型速度为 2 m/s,而咳嗽时释放的液滴大小不同,典型速度为 20 m/s s,进入典型的房间气流速度 <0.25 m/s。因此,简单地提及液滴而不是大液滴并使用气溶胶可能更好指小到足以悬浮在空气中一段时间​​的液滴。值得注意的是,室内空气中的气溶胶直径大多为 5 µm 或更小,而呼出喷射中的气溶胶要大得多(直径12 ≤ 50 µm )。

附带说明一下,世卫组织和美国疾病预防控制中心都认为,防止呼吸道病原体传播的预防措施包括防止接触、飞沫和空气传播的措施,除了标准预防措施外,还应实施这些措施。3, 4通常说,实施这些预防措施中的几项比单独的预防措施更重要,这证明可能存在多种传播途径,哪些传播途径最突出存在不确定性,以及传播途径的定义存在一些歧义。因此,如果可以更明确地定义传播途径,从而可以采取更准确的预防措施,将会有所帮助。

上面描述的经典分类在概念上是有用的,但它基于想象和推理,而不是对分类标准的系统考虑。在呼吸飞沫的产生、释放、运输和暴露途径方面获得的新知识使这一分类得以修订。传播途径的良好分类应该没有歧义或不一致,以便公共卫生专家可以制定一致的预防和预防政策,并且多个学科的研究人员可以轻松地将他们的知识应用和整合到传播机制和干预措施的研究中。还应根据对传播机制的最新机制理解更新传播途径分类,

气溶胶、污染物和大液滴传播的现有概念是基于病原体颗粒的位置(即,在空气中、污染物上或在/或液滴中),而不是它们如何转移(传播)。大飞沫传播和密切接触传播在空气喷射理论出现之前就被提出,后者现在已被广泛用于理解呼吸活动(如咳嗽和正常呼吸)中呼出的气流。此外,在能够区分建筑物中的空气分布模式之前,飞沫核10的空气传播的概念已经得到很好的发展。

下面,我们提出了一套以传播过程为重点的标准,用于对呼吸道病毒的基本传播途径进行分类。括号内为所涉及的媒体,我们在这个新的分类中采用了“媒体+传输”的结构。

  1. (滴)喷雾传播是指呼吸道病毒通过感染者排出的载有病毒的液滴喷洒在易感者的粘膜表面(例如,眼睛、鼻子和嘴巴)上而传播。因此,只有移动的液滴才能通过这个过程传播病毒,这种移动是由于在释放点(例如在口中)获得的动力。由于呼出气流的性质,这种液滴喷雾传输只能在一定的范围内进行。蔡平9写道:“大多数疾病不太可能是通过灰尘传播的,它们只能通过两到三英尺的喷雾传播,毕竟这种现象更像接触感染,而不是通常理解的空中感染。” 液滴喷雾传输与传统的大液滴传输相同,但避免使用含糊不清的“液滴”术语,“喷雾”一词增强了理解:很容易想象面罩被用来阻挡喷雾,或面罩被用来阻挡滴。
  2. (气溶胶)吸入传播是指空气悬浮的载有病毒的呼吸道飞沫被感染者呼出并被易感者吸入。气溶胶吸入可发生在短程和长程。当易感者靠近感染者时,即在 1-2 m 内,通过气溶胶吸入传播的风险更大。流动的空气可以四处传播呼吸气溶胶,但静止的空气不能。然而,一个人可能会从含有静止空气的房间吸入含有病毒的气溶胶,因为吸入本身就是一个气流过程。
  3. (表面)接触传播是指有生命的(例如,皮肤)或无生命的(污染物)表面存在病毒的呼吸道飞沫或飞沫被人手触摸此类表面并随后触摸他/她的粘膜,从而导致自身接种。

这三个新定义的途径可以被认为是三种基本的病毒传播途径。显然,第四种传播途径是含有病原体的体液的直接传播(例如,接吻)。虽然喷雾传播只能在近距离接触时发生,但吸入和接触传播都可以在长距离内发生。这三个基本的传递过程也满足了分类的基本原则之一,即认知经济,即“以最少的认知努力提供最多的信息”。13这些过程可能适用于对由其他机制(例如,医用气溶胶或粪便气溶胶)产生的气溶胶传播进行分类,前提是它们在特定病原体的传播中发挥作用。

根据共同的关系或属性,如感染环境、感染者与易感者之间的距离、传播媒介或携带病毒的飞沫或气溶胶的来源,可以进一步对传播途径进行分类。

关于距离,有两种类型的传播:近距离接触传播(近距离或短距离,即距离感染者 1-2 m 以内)和远距离传播(长距离,即距离感染者 >1-2 m)。感染者)(图1)。至关重要的是,我们的定义阐明了病毒传播的所有三种基本途径,即喷雾、吸入和接触传播,都可以参与密切接触传播。接近吸入传播在文献中被称为“短程气溶胶传播”,而接近接触传播被称为“直接表面”途径。6然而,关于密切接触传播,美国疾病预防控制中心和世卫组织基于传播的预防方法3、4不考虑近距离吸入途径,尽管这很可能发生并且可能占主导地位。吸入和基于触摸的传播都是远程传播的可能形式。最后,近距离吸入的气溶胶比远距离吸入的气溶胶大。

图片
图1
在图形查看器中打开微软幻灯片软件
室内三种基本短距离传播途径(喷雾、吸入和接触)和长距离传播(吸入和接触)的图示。过期的喷射范围显示为浅绿色,感染者显示为红色,易感者显示为蓝色(从14修改)。水滴显示为大黑圈,气溶胶显示为小黑圈
更新日期:2021-01-21
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